Pediatric Radiology

, Volume 42, Issue 7, pp 775–784

Maximizing time-resolved MRA for differentiation of hemangiomas, vascular malformations and vascularized tumors

Authors

    • Department of RadiologyMontefiore Medical Center
  • Alexander Chandler
    • Department of RadiologyMontefiore Medical Center
  • Ross Borzykowski
    • Department of RadiologyMontefiore Medical Center
  • Beverly Thornhill
    • Department of RadiologyMontefiore Medical Center
  • Benjamin H. Taragin
    • Department of RadiologyMontefiore Medical Center
Review

DOI: 10.1007/s00247-012-2359-5

Cite this article as:
Kim, J.S., Chandler, A., Borzykowski, R. et al. Pediatr Radiol (2012) 42: 775. doi:10.1007/s00247-012-2359-5

Abstract

Contrast-enhanced magnetic resonance angiography (MRA) using time-resolved imaging is a relatively new and increasingly popular technique. We will describe the technique utilized at our institution, Time-Resolved Imaging of Contrast Kinetics (TRICKS; GE Healthcare, Milwaukee, WI), and the parameters that can be adjusted to optimize the exam. We will review key imaging features of hemangiomas and vascular malformations in various modalities, with a special emphasis on the TRICKS appearance.

Keywords

MRATRICKSHemangiomasVascular malformationsChildren

Introduction

The misclassification of vascular anomalies remains common, despite fundamental pathological differences. Many of the patients referred to our institution for vascular anomalies arrive with an inaccurate diagnosis. One of the most common diagnostic confusions is the distinction between hemangiomas and venous vascular malformations. Additionally, in some cases, vascular anomalies may even be confused with highly vascularized solid tumors.

In 1982, Mulliken and Glowacki [1] proposed a classification of vascular anomalies based on endothelial, histological and clinical characteristics into two basic categories of hemangiomas and vascular malformations. Hemangiomas are characterized by a hypercellular and rapidly proliferating phase followed by an involuting phase with diminished cellularity, whereas vascular malformations demonstrate normal cell turnover rate, grow commensurate with the size of the body and do not regress spontaneously.

Vascular malformations represent the abnormal persistence of embryonic vessels, and can be further subclassified according to the type of vessel: capillary, arterial, venous, lymphatic, or mixed. In contrast to hemangiomas, they expand continuously throughout life due to constant hydrostatic pressure within the vessels, may expand more rapidly under the influence of hormones produced during puberty or pregnancy, and show no pattern of regression later in life [1, 2]. Alternatively, vascular malformations may be classified based on the presence of high-flow versus low-flow vessels, with those containing arterial components classified as high-flow [3].

An accurate distinction between hemangiomas and vascular malformations is important as the management of these two entities is entirely different [2]. Though most hemangiomas spontaneously resolve, approximately 10–20% will warrant pharmacological, surgical or laser intervention [2, 46]. In contrast, percutaneous sclerotherapy or more invasive transarterial embolization is used to treat vascular malformations depending on whether the lesion is high-flow or low-flow [7].

The diagnosis of hemangiomas or vascular malformations is most often a clinical one. Radiologic imaging plays a role in challenging cases and can be used to assess the depth and extent of the lesion [7]. US and MRI remain the two primary imaging modalities used to characterize vascular anomalies. High-resolution gray-scale and Doppler US provide excellent characterization of superficial structures and hemodynamics. However, MRI is the single best exam for vascular anomaly diagnosis, due to its strong soft-tissue contrast and ability to define the extent of the lesion and involvement with nearby structures.

MRA is emerging as a reasonable alternative to conventional diagnostic catheter angiography [8]. Advantages over conventional angiography include lack of ionizing radiation and a lower degree of invasiveness with its associated complications. Due to the lengthy time of examination and artifactual signal loss with time-of-flight acquisition, contrast-enhanced MRA has become more widely used.

Although contrast-enhanced MRA may distinguish arterial from venous components of the vascular anomaly, the exam can be technically challenging due to the variability of contrast arrival in the distal extremities [9]. Time-Resolved Imaging of Contrast Kinetics (TRICKS) is a method that solves the issue of timing.

Rather than sample all spatial data for each time frame, TRICKS uses an algorithm to sample lower spatial frequencies more often than higher spatial frequencies, and estimates missing data by linear interpolation of values from shared data across time frames. This improves the temporal resolution; however, the spatial resolution is decreased [9, 10]. With high temporal resolution, images that coincide with contrast uptake in the area of interest can be obtained with the course of blood flow through arterial, capillary and venous phases [911].

Other advantages of TRICKS over conventional contrast-enhanced MRA include elimination of a timing run with the contrast agent [8]. This allows the use of a smaller dose of contrast material with all of the injected contrast agent dedicated toward imaging [8, 9]. TRICKS also has the ability to cover a large region in children allowing comparison with the contralateral side. In one study, TRICKS was shown to have faster in-room time requirements (less than 30 min on average) than angiography, venography or duplex sonography [12].

Technique

At our institution, an intravenous line is positioned in the upper extremity opposite the lesion being imaged to avoid injecting an involved vein. The affected and unaffected sides of the child are included in the field of view for evaluation in a single plane. For distal upper extremity lesions, the hands of the child are placed above the head in a “superman” position to avoid wraparound artifact. Any extension tubing must be excluded from the field of view (Fig. 1). Standard gadolinium-based intravenous agents may be used. However, we have moved with greater frequency to off-label use of a gadolinium-based blood-pool contrast agent gadofosveset trisodium (Ablavar – formerly Vasovist; Lantheus Medical Imaging, North Billerica, MA) to prolong the intravascular phase. A saline flush is administered to clear the contrast agent from the IV tubing, which is even more important in pediatric cases where a small amount of contrast material is used.

The best plane for image acquisition of vascular malformations is the coronal plane. As TRICKS is a 3-D acquisition, postprocessing reconstructions can be performed in the axial and sagittal planes. At our institution, an initial mask sequence is obtained. The initiation of scanning occurs before the injection of contrast agent to capture early arterial information and to safeguard against contrast wastage in the event of scanner malfunction. We typically perform 15 phases in children, and up to 30 phases for peripheral lesions in adults to ensure acquisition of the venous phase. If the patient moves during the scan, we simply acquire another mask sequence, reinject the patient and repeat the scan as the original gadolinium will be subtracted from the second mask sequence.

Optimization of the temporal resolution is very important, and should be adjusted on a case-by-case basis. While increasing temporal resolution allows better separation of the arterial and venous phases, decreasing temporal resolution can be helpful in suspected peripheral venous lesions, and in patients with slow peripheral flow such as those with decreased cardiac output and bradycardia. Therefore, these parameters should be adjusted based on the likely pretest diagnosis, formulated from physical exam and US, and with consideration of the patient’s age and cardiac output.

There are several parameters that can be used to increase the temporal resolution of TRICKS sequences. Decreasing both the phase and frequency encoding steps will increase temporal resolution at the expense of spatial resolution. Another option is increasing the bandwidth, which lowers the signal-to-noise ratio. Finally, decreasing the number of slices will also increase temporal resolution.

The TRICKS study is obtained within the context of a complete diagnostic examination (Table 1). Our protocol is designed to maximize anatomical information and characterize the dynamic nature of the vascular supply. Spin echo precontrast sequences are utilized to accentuate flow voids in high-flow vessels. Coronal and axial T1 sequences both provide fine anatomical detail of soft-tissue and bony involvement. An axial T1 with FS sequence is performed for comparison with a later postcontrast sequence. Coronal T2 with and without fat saturation and axial T2 with fat saturation both aid in characterization of lesion content. Finally, the coronal gradient echo sequence can detect blooming artifact, which is characteristic of phleboli. Contrast agent is then injected with a minimum of 15 phases of TRICKS acquisition followed by an axial T1 sequence with FS to visualize the conventional postcontrast appearance of the lesion. We feel that analyzing the TRICKS vascular pattern and the axial T1 with FS postcontrast enhancement can significantly help differentiate hemangiomas from vascular malformations and from other vascularized tumors.
Table 1

MR imaging protocol for 1.5-T systems

Parameter

Coronal T1

Coronal T2 with and without FS

Coronal gradient echo

Axial T1 with and without FSa

Axial T2 with FS

TRICKS

TR/TE (msec)

475/20

4,000/102

425/17

475/20

4,000/102

5.9/2

Flip angle (degrees)

20

45

Section thickness (mm)

3

3

3

5

5

1.6

NEX

2

2

2

2

2

0.5

Matrix

224 × 256

224 × 256

192 × 256

224 × 256

224 × 256

256 × 320

FOV (mm)

variable

variable

variable

15–24

15–24

480

No. of sections

24–30

24–30

24–30

40–50

40–50

30–40

Imaging time (sec)

300

240 270 (with FS)

360

300–420 360–540 (with FS)

270

20 × number of phases

FOV field of view, FS fat saturation, NEX number of excitations, TE echo time, TR repetition time

aPostcontrast TRICKS images were obtained with the same sequence

Hemangiomas

Hemangiomas are benign blood vessel tumors, theorized to have originated from placental tissue embolized into the fetal circulation, and are divided into two subtypes: congenital and infantile. Congenital hemangiomas have already reached their maximal growth at birth and are characterized by their pattern of involution with rapidly involuting congenital hemangiomas (RICH) showing a remarkable rate of regression after birth and non-involuting congenital hemangiomas (NICH) persisting with seemingly no natural course of regression [13]. Infantile hemangiomas (IH) are the most common tumors found in infants, typically appearing within the first few weeks of life [3, 14]. They undergo a proliferative phase of rapid growth until about 8–12 months of age, at which point involution begins with a highly variable time course over the next several years.

Hemangiomas are most often found in the head and neck with the clinical appearance depending on the depth and phase of growth. They are more likely to be found in females and Caucasians [14]. The most common complication of hemangiomas is ulceration, which can lead to infection and scarring. Other complications are related to impingement of nearby vital organs such as the orbits, airway and spine [4].

On US, hemangiomas generally appear as well-circumscribed, non-infiltrating soft-tissue masses. They may be hyperechoic and/or hypoechoic with increased color flow on Doppler (Fig. 2). On MRI, hemangiomas are iso- or hypo-intense to muscle on T1-W images, hyperintense on T2-W images, and contain flow voids indicating the presence of high-flow vessels [3, 6, 15].
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Fig. 1

Left chest wall hemangioma in a 3-month-old. Coronal TRICKS image demonstrates an avid, homogenously enhancing mass (single arrow), initially visualized in phase 2 of 15, concurrent with arterial vessels. Note the wraparound artifact of the child’s hands from improper positioning, and the extension tubing from the child’s intravenous line, which may mimic a vessel (double arrows)

TRICKS demonstrates avid, homogeneous, early arterial enhancement without neovascularity and should not demonstrate an early draining vein (Figs. 1 and 2). Venous drainage will be concurrent with that of the surrounding local structures [12]. This pattern is useful to distinguish hemangiomas from enhancing solid tumors, which will enhance on later arterial and/or early venous phases. Post-TRICKS T1-W with FS sequences will demonstrate a uniform pattern of contrast enhancement. The lack of neovascularity and the presence of uniform enhancement differentiate hemangiomas from malignant tumors [3, 11, 15].
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Fig. 2

Left gluteal hemangioma in a 2-year-old girl. a Spectral color Doppler US image demonstrates a well-defined heterogenous mass with arterial waveform. b Sagittal T1-W with fat saturation postcontrast MRI demonstrates avid and homogenous enhancement of the mass. c Reconstructed image from a coronal TRICKS acquisition shows avid, early enhancement of the mass in phase 4 of 15, concurrent with arterial enhancement and without evidence of an early, dilated draining vein

During involution of hemangiomas, there is decreasing vascularity and enhancement with fibrofatty replacement. This fatty change is easily recognized on MR as increasing high signal on T1-W images [3]. This may be confused with underdevelopment of tissues related to the steal phenomenon characteristically seen in AVMs. After involution, there is no contrast enhancement, and the peripheral vessels decrease in size [3].

Hepatic hemangioma or hemangioendothelioma is a type of infantile hemangioma that has a similar MR imaging appearance, characteristically hypointense on T1-W sequences and uniformly hyperintense on T2-W sequences (Fig. 3). These lesions are usually associated with vascular flow voids. However, in contrast to early uniform enhancement seen in peripheral hemangiomas, TRICKS imaging of hepatic hemangiomas typically demonstrates early centripetal enhancement (rim enhancement with gradual filling of the center of these lesions) with variable degrees of central non-enhancement corresponding to necrosis. Arteriovenous and portovenous anastamoses as well as a large central varix are present in some lesions [16].
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Fig. 3

Multiple liver hemangiomas in a 1-month-old. a Axial T1-W with fat saturation image demonstrates a large iso- to hypointense mass in the right hepatic lobe with multiple low areas of signal abnormality (arrows), representing flow voids and a smaller hypointense lesion in the caudate lobe. b Axial T2-W with fat saturation image demonstrates these lesions to be hyperintense with the presence of additional smaller lesions. c Coronal TRICKS image demonstrates avid peripheral enhancement (arrow) in phase 3 of 34, concurrent with arterial vessels. Early venous enhancement of the IVC (arrowhead) indicates arteriovenous shunting (Images are courtesy of Dr. Sarah Sarvis Milla, NYU Medical Center)

Kaposiform hemangioendothelioma

Kaposiform hemangioendothelioma (KHE) is an aggressive, histologically distinct variant of hemangiomas with spindle-shaped endothelium, microthrombi, hemosiderin deposits and an infiltrative growth pattern [3, 11, 17]. These lesions are often complicated by the life-threatening Kasabach-Merritt phenomenon, marked by profoundly decreased peripheral blood platelets and fibrinogen due to platelet trapping and spontaneous hemorrhage [3, 17]. They most often appear as ill-defined, purpuric masses and are most commonly found in the midline of the trunk, extremities and retroperitoneum [3, 11, 17]. Acquired tufted hemangiomas are thought to be on the same neoplastic spectrum as KHEs, with overlapping histological features and somewhat higher-than-average platelet counts [17].

KHEs generally appear as ill-defined soft-tissue masses with variable echogenicity on US. Calcifications may be present, which are not seen in infantile hemangiomas [6]. In contrast to a typical hemangioma, KHEs characteristically have poorly defined soft-tissue encapsulation, involving multiple tissue planes with skin thickening, subcutaneous edema and stranding [11] (Fig. 4). The presence of signal voids may be related to hemosiderin or other blood products, or to fibrosis. Unlike in infantile hemangioma, destructive bony involvement is common in KHEs [6]. KHEs are hypervascular with high-flow vessels, but, in contrast to hemangiomas, the vessels are less prominent [3].
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Fig. 4

Thrombocytopenia and leg swelling with a kaposiform hemangioendothelioma in a 3-month-old girl. a Axial T2-W with fat saturation MR demonstrates an ill-defined mass with extensive surrounding soft-tissue edema (M = marker capsule). b Coronal T1-W with fat saturation postcontrast MR demonstrates avid, heterogeneous enhancement of the mass. c Coronal TRICKS MRI demonstrates early enhancement in phase 6 of 15, concurrent with arterial enhancement of an ill-defined mass from a dilated feeding vessel (arrow)

On TRICKS, there is a distinct feeding vessel similar to conventional hemangiomas. However, the early arterial enhancement is heterogeneous and less avid than that of a typical hemangioma. On the post-TRICKS T1-W with FS sequence, there is surrounding enhancement in the invaded and edematous soft tissues (Fig. 4).

Venous malformations

Venous malformations (VMs) are the most common type of vascular malformation, accounting for one-half to two-thirds of all cases [15]. They are typically found in the head and neck regions or extremities, and present as easily compressible soft-tissue masses [7]. They are often painful with venous engorgement [3, 11].

On US, venous malformations demonstrate mixed echogenicity with compressible, low-flow vessels [3, 6]. In contrast to hemangiomas, the slow blood flow and subsequent intralesional thrombosis in these lesions may produce phleboli detectable on CT [15]. On MR imaging, VMs are typically hypo- to isointense to muscle on T1, although the presence of heterogeneity may indicate hemorrhage or thrombosis. High signal on T2-W imaging is characteristic, with septations or thrombosis producing areas of low signal. Phleboli, occasionally seen in hemangiomas, are much more common in venous malformations and may produce signal voids on T2-W and gradient echo sequences [3, 6, 7]. The presence of patchy but confluent areas of enhancement differentiates VMs from poorly enhancing lesions such as lymphatic malformations. In the venous phase of conventional angiography, contrast agent may puddle in the sinusoidal spaces [3, 11].

During TRICKS imaging, there is delayed enhancement of the venous spaces and tortuous vessels with the absence of venous shunting [7, 12] (Fig. 5). Namely, the lesion will remain unenhanced during the arterial phase and will only enhance during the venous phase. Although there is commonly an enlarged draining vein with dilatation of the major surrounding veins, there is no intra-lesional shunting or early venous filling. The post-TRICKS T1-W with FS images will demonstrate complete enhancement with the exception of signal voids related to phleboli.
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Fig. 5

Images in a 15-year-old who presented with a left neck venous malformation. a Sagittal T2 with fat saturation MRI demonstrates a hyperintense mass (arrow) with multiple areas of low signal abnormality representing phleboli. b Sagittal T1-W with fat saturation postcontrast MR reconstructed images demonstrate a centrally enhancing mass. c Sagittal reconstruction from a coronal acquisition TRICKS MR image shows delayed enhancement in phase 9 of 15, concurrent with venous structures and the presence of dilated draining veins (arrows)

Arteriovenous malformations

Demonstrating artery-to-vein connections via intervening dysplastic vessels, arteriovenous malformations (AVMs) compose 10% of all vascular malformations. They often become symptomatic during puberty under the influence of hormonal changes and are marked clinically as pulsatile, warm areas of superficial blushing. The shunting in AVMs may ultimately cause tissue ischemia, leading to pain and ulceration of the skin [15].

On imaging, an AVM does not appear as a discrete mass, but rather a nidus of confluent, dilated vessels with arteriovenous shunting [3, 11]. These dilated vessels may be appreciated on angiography, with early opacification of enlarged draining veins [3]. US demonstrates high-flow vessels with low arterial resistance and a higher venous peak velocity than other vascular malformations or hemangiomas [18] (Fig. 6). In contrast to hemangiomas, there is arterialization of the draining veins with pulsatile flow [6]. Signal voids are typically present on both T1-W and T2-W images with high-flow vessels demonstrating high signal on gradient echo (Fig. 6).
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Fig. 6

Right scapular AVM in a 12-week-old girl. a Spectral color Doppler US image demonstrates a waveform typical for low arterial resistance with arterialization of the draining veins. (b) Coronal T1 with fat saturation postcontrast MR images demonstrate avid enhancement of the lesion. c Coronal TRICKS MRI demonstrates the presence of early, dilated draining veins (arrows), which enhance in phase 7 of 15, concurrent with arterial vessels, indicating arteriovenous shunting

TRICKS demonstrates early enhancement with early venous shunting through the nidus with good enhancement on first pass of the feeding arteries and dilated draining veins [7, 12] (Fig. 6). A steal phenomenon may be observed with preferential flow to the AVM, causing underdevelopment and atrophy of nearby musculoskeletal structures. The post TRICKS T1-W with FS sequence reveals enhancing vascularity but no defined soft-tissue mass.

Lymphatic malformations

Lymphatic malformations (LMs) are composed of chylous fluid, lined by endothelium. They can be characterized as macrocystic or microcystic, commonly referred to as lymphangioma or cystic hygroma, respectively. Microcystic LMs are composed of numerous small cysts of less than 2 cm, whereas macrocystic LMs have cysts of larger and varying size [19]. Most LMs are present at birth with 90% seen at 2 years of age [15]. The most common location for LMs is the head and neck and, on examination, lymphatic malformations are rubbery and noncompressible [3, 7, 15].

On US, macrocystic LMs appear as multiloculated cystic lesions with vascular flow in the septa (Fig. 7). Pure microcystic LMs appear ill-defined and hyperechoic, due to the innumerable interfaces produced by the tiny cysts. Classically, due to the fluid content, there is low signal on T1-W and intense high signal on T2-W MR imaging. However, increased T1 signal and fluid/fluid levels may be present due to proteinaceous or hemorrhagic content. Lymphedema may manifest as adjacent subcutaneous fat stranding.
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Fig. 7

Right chest wall macrocystic LM in a 10-week-old girl. a Color Doppler US image demonstrates a complex cystic mass (arrows) with no internal vascular flow. b Axial T1-W with fat saturation postcontrast image demonstrates a cystic mass with peripheral enhancement (arrows) suggestive of superimposed infection. c Coronal TRICKS MRI shows slightly enlarged intercostal arteries and peripheral enhancement of the lesion (arrow) in phase 11 of 35. d Magnified coronal oblique reconstructed image also demonstrates peripheral enhancement with slightly enlarged intercostal arteries (arrows)

TRICKS imaging may show enlarged feeding vessels, but as opposed to hemangiomas, the overwhelming majority and center of the lesion will never enhance (Fig. 7). There may be enhancement of the septations, but no early venous drainage. Post-TRICKS T1-W with FS images will show only rim or septal enhancement in macrocystic LMs, while microcystic LMs typically have no enhancement.

Approach to diagnosis

The clinical history and US and MRI characteristics may help distinguish hemangiomas from vascular malformations and other vascularized tumors. However, many of these entities demonstrate similar precontrast MR characteristics of hypointensity on T1-W and hyperintensity on T2-W sequences. We propose an algorithm that relies heavily on the postcontrast T1-W FS images along with the temporal enhancement pattern visualized during TRICKS (Fig. 8).
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Fig. 8

Algorithm shows pathway designed to facilitate diagnosis

In our algorithm, the first step is to determine whether there is avid, early arterial enhancement or minimal to moderate arterial enhancement on the T1-W FS postcontrast images. Next, the decision tree utilizes the TRICKS enhancement pattern and other definable enhancement characteristics including dilated veins, septations and arteriovenous shunting. Combining this information will lead to a more confident diagnosis of one of the entities previously described. The algorithm can also help identify lesions that do not fit established criteria (Figs. 9 and 10) and where tissue sampling may be indicated (Fig. 9).
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Fig. 9

Right arm low-grade sarcoma in a 22-year-old woman. a Coronal T1-W with fat saturation postcontrast MRI shows an avidly enhancing soft-tissue mass (arrow). b Coronal TRICKS MRI demonstrates enhancement of tortuous, haphazardly arranged vessels, suggestive of neovascularity in phase 8 of 10 without evidence of early arterial enhancement or presence of a dilated draining vein. c Magnified coronal oblique reconstructed image better demonstrates findings suggestive of neovascularity of the lesion

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Fig. 10

Images in a 3-year-old who presented with neck bulging when crying with ectasia of the left internal jugular vein. a Axial double inversion recovery image demonstrates a dilated left internal jugular vein depicted as a flow void (arrow). b Coronal TRICKS MRI demonstrates enhancement of the left internal jugular vein (arrow) in phase 7 of 15

The presence of neovascularity, defined here as tortuous vessels that are purposeless in direction and show no progressive diminution in caliber, can also aid in distinguishing benign from malignant tumors (Fig. 9). However, it can be difficult to differentiate neovascularity from abnormal vascularity present in benign lesions such as certain types of hemangiomas [20]. Fortunately, many of these entities can be classified by other imaging characteristics and clinical information.

Conclusion

The distinction between hemangiomas, vascular malformations and other vascularized tumors is important, as they are managed by different treatment regimens. Though these lesions are often diagnosed clinically, the challenge of doing so results in a substantial rate of misdiagnoses. Through a series of illustrative cases, and an approach to diagnosis algorithm, we have demonstrated our method of differentiating these lesions by maximizing the temporal enhancement pattern of vessels that TRICKS imaging so nicely demonstrates.

Copyright information

© Springer-Verlag 2012