Maximizing Time Resolved MRA for Differentiation of Hemangiomas,

Vascular Malformations, and Vascularized Tumors

Jane S. Kim MD, Linda Y. Kao MD, Ross Borzykowski MD, Benjamin H. Taragin MD

Montefiore Medical CenterBronx, NY

Goals and Objectives

• Provide background information on contrast-enhanced Magnetic Resonance Angiography (MRA) using time resolved imaging for vascular anomaly diagnosis

• Describe the technique used at our institution and optimization of exam parameters

• Review key imaging features of hemangiomas and vascular malformations in various modalities with special emphasis on the TRICKS appearance

• Propose a diagnostic algorithm that relies heavily on the post contrast T1 with fat saturation post TRICKS enhancement appearance and the temporal TRICKS enhancement pattern

Introduction

• Misclassification of vascular anomalies remains common despite fundamental pathologic differences

• An accurate distinction is important for management:– Though most hemangiomas spontaneously resolve, approximately 10-

20% will warrant pharmacologic, surgical, or laser intervention– Percutaneous sclerotherapy or more invasive transarterial

embolization is used to treat vascular malformations depending on whether the lesion is high-flow or low-flow

Mulliken and Glowacki Classification

Hemangiomas• characterized by a hypercellular

and rapidly proliferating phase followed by an involuting phase with diminished cellularity

• further sub-classified:– Congenital hemangiomas

• Rapidly Involuting Congenital Hemangiomas (RICH)

• Non-Involuting Congenital Hemangiomas (NICH)

– Infantile hemangiomas

Vascular Malformations• demonstrate normal cell turnover

rate, grow commensurate with the body, and do not regress spontaneously

• further sub-classified according to type of vessel: capillary, arterial, venous, lymphatic, or mixed

• may also be classified based on presence of high-flow versus low-flow vessels, with those containing arterial components classified as high-flow

Vascular Anomaly Diagnosis• Most often a clinical diagnosis • Radiologic imaging provides a

role in challenging cases and can be used to assess the depth and extent of the lesion– Ultrasound: provides

excellent characterization of superficial structures and hemodynamics

– MRI: single best exam due to its strong soft tissue contrast and ability to define extent of the lesion and involvement with nearby structures

http://www.adhb.govt.nz/newborn/teachingresources/dermatology/VascularLesions.htm

Contrast-Enhanced MR Angiography

• Emerging as a reasonable alternative to conventional diagnostic catheter angiography

• Advantages include lack of ionizing radiation and a lower degree of invasiveness with its associated complications

• Can be technically challenging due to the variability of contrast arrival in the distal extremities

Time-Resolved Imaging of Contrast Kinetics (TRICKS, GE Healthcare)

• Algorithm samples lower spatial frequencies (center of k-space) more often than higher spatial frequencies (periphery of k-space)

• Estimates missing data by linear interpolation of values from shared data across time frames

• Improves temporal resolution at the expense of spatial 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

Advantages of TRICKS over conventional Contrast-Enhanced MR Angiography

• Elimination of a timing run with the contrast agent – Allows use of a smaller dose of contrast material with all injected

contrast dedicated towards imaging

• Ability to cover a large region in pediatric patients allowing comparison with the contralateral side

• In one study, TRICKS was shown to have faster in-room time requirements (less than 30 minutes on average) than angiography, venography, or duplex sonography

Our Technique• IV line placed in the upper

extremity opposite to the lesion being imaged to avoid injecting an involved vein

• Both affected and unaffected sides of the patient included in the field of view for evaluation in a single plane

• For distal upper extremity lesions, the patient’s hands placed above the head in a “superman” position to avoid wraparound artifact

• Any extension tubing must be excluded from the field of view Coronal TRICKS image demonstrates an avid, homogenously

enhancing mass (arrow), initially visualized in phase 2 of 15, concurrent with arterial vessels. Note the wraparound artifact of the patient’s hands from improper positioning, and the extension tubing from the patient’s intravenous line, which may mimic a vessel (double arrows)

3 month old with a left chest wall hemangioma

Contrast administration

• Standard gadolinium-based intravenous agents may be used• Gadolinium based blood-pool contrast agent Gadofosveset

Trisodium (Ablavar – formerly Vasovist; Lantheus Medical Imaging; North Billerica, MA) typically used (off-label) at our institution in order to prolong the intravascular phase

• A saline flush is administered to clear the contrast from the IV tubing (even more important in pediatric cases where a small amount of contrast is used)

Image Acquisition• Best performed in the coronal plane with post-processing in the

axial and sagittal planes• Initial mask sequence obtained with initiation of scanning before

the injection of contrast in order to:– capture early arterial information– safeguard against contrast wastage in the event of scanner malfunction

• Typically perform 15 phases in our pediatric population, and up to 30 phases for peripheral lesions in our adult population to ensure acquisition of the venous phase

• If the patient moves during the scan, we simply acquire another mask sequence, re-inject the patient, and repeat the scan as the original gadolinium will be subtracted from the second mask sequence

Optimization of Temporal Resolution

• Should be adjusted on a case-by-case basis– 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

• Temporal resolution can be increased by:– Decreasing both the phase and frequency encoding steps (at the

expense of spatial resolution)– Increasing the bandwidth (lowers signal-to-noise ratio) – Decreasing the number of slices

Complete MR diagnostic exam• Spin echo pre-contrast sequences utilized to accentuate flow voids in high

flow vessels • Coronal and axial T1 sequences both provide fine anatomic detail of soft

tissue and bony involvement • Axial T1 with FS sequence performed for comparison with a later post-

contrast sequence • Coronal T2 with and without FS and axial T2 with FS both aid in

characterization of lesion content • Coronal gradient echo sequence detects blooming artifact, characteristic

of phleboli • Contrast is injected with a minimum of 15 phases of TRICKS acquisition

followed by an axial T1 sequence with FS in order to visualize the conventional post-contrast appearance of the lesion

Typical MR Imaging Protocol for 1.5-T Systems

Parameter Coronal T1Coronal T2 with and without FS

Coronal gradient echo

Axial T1 with and without FS* Axial T2 with FS TRICKS

TR/TE (msec) 475/20 4000/102 425/17 475/20 4000/102 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 x 256 224 x 256 192 x 256 224 x 256 224 x 256 256 x 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

20sec x number of phases

Note: FOV = Field of View, FS = Fat Saturation, NEX = Number of excitations, TE = echo time, TR = repetition time*Postcontrast TRICKS images are obtained with the same sequence

Approach to Diagnosis

• Clinical history, US and MRI characteristics often helpful; however, many entities demonstrate similar precontrast MR characteristics

• Our algorithm relies heavily on the post contrast T1W FS images and the TRICKS temporal enhancement pattern:1. Determination of avid, early arterial enhancement or minimal to

moderate arterial enhancement on T1W FS post contrast images2. TRICKS temporal enhancement pattern3. Other definable enhancement characteristics including dilated veins,

septations, and arteriovenous shunting

Can also help identify lesions that do not fit established criteria and where tissue sampling may be indicated

Peripheral EnhancementPeripheral Enhancement

Central EnhancementCentral Enhancement

Minimal to Moderate Enhancement Avid Enhancement

Early Arterial EnhancementEarly Arterial Enhancement

Late Arterial/Venous EnhancementLate Arterial/Venous Enhancement

TRICKS Enhancement

Pattern

T1W with FS post TRICKS Enhancement

Not definitely a vascular

malformation

AVM HemangiomaMicrocystic LM vs. Tumor with

Hemorrhage

Macrocystic LM

Venous Malformation

Presence of early dilated draining veins

Yes No

Presence of dilated veins

Rim Type

Heterogeneous and septated

Algorithm

Hemangiomas• Benign blood vessel tumors, theorized to have originated from

placental tissue embolized into the fetal circulation • Most often found in the head and neck with clinical appearance

depending on the depth and phase of growth • Further sub-classified into 2 subtypes:

– Congenital Hemangiomas: maximum growth at birth• RICH: remarkable rate of regression after birth• NICH: demonstrates growth to that of the child without regression

– Infantile Hemangiomas: most common tumor of infancy• Undergoes proliferative phase of rapid growth until 8-12 months with variable rate

of regression over the next several years

• During involution, there is decreasing vascularity with fibrofatty replacement

Hemangiomas: Imaging• US:

– Well-circumscribed hyperechoic and/or hypoechoic soft tissue mass with color doppler flow

• MR: – Iso- or hypo-intense on T1W– Hyperintense on T2W– Flow voids due to high flow vessels– Fatty change during involution with

high T1 signal

• TRICKS:– avid, homogenous, early arterial

enhancement without neovascularity– should not demonstrate an early

draining vein

• Post TRICKS T1W with FS:– uniform pattern of contrast

enhancement

Case 1: 2 year old female with a left gluteal hemangioma

Spectral color doppler US image demonstrates a well-defined heterogenous mass with arterial waveform Sagittal T1W with fat saturation post contrast

MR image demonstrates avid and homogenous enhancement of the mass

Case 1: 2 year old female with a left gluteal hemangioma 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

Kaposiform Hemangioendothelioma (KHE)

• aggressive, histologically distinct variant of hemangiomas with an infiltrative growth pattern

• 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

• most commonly found in the midline of the trunk, extremities, and retroperitoneum as an ill-defined, purpuric mass

• Acquired tufted hemangiomas thought to be on the same neoplastic spectrum as KHEs

Kaposiform Hemangioendothelioma: Imaging

• US:– Ill-defined soft tissue mass with

variable echogenicity– Calcifications may be present

• MR:– Poorly defined soft tissue

encapsulation involving multiple tissue planes with skin thickening, subcutaneous edema and stranding

– Signal voids may be related to hemosiderin or fibrosis

– Destructive bony involvement is common

• TRICKS:– early arterial enhancement is

heterogenous and less avid than that of a typical hemangioma

• Post TRICKS T1W with FS:– surrounding enhancement in the

invaded and edematous soft tissues

Case 2: 3 month old female with thrombocytopenia and leg swelling with a kaposiform

hemangioendothelioma

Axial T2W with fat saturation MR demonstrates an ill-defined mass with extensive surrounding soft tissue edema (M = Marker capsule) Coronal T1W with fat saturation post contrast

MR demonstrates avid, heterogenous enhancement of the mass

Case 2: 3 month old female with thrombocytopenia and leg swelling with a KHECoronal TRICKS MR image demonstrates early enhancement in phase 6 of 15, concurrent with arterial enhancement of an ill-defined mass from a dilated feeding vessel (arrow)

Venous Malformations

• most common type of vascular malformation, accounting for one-half to two-thirds of all cases

• typically found in the head and neck region or extremities• present as easily compressible soft tissue masses often

painful with venous engorgement

Venous Malformations: Imaging• US:

– Mixed echogenicity with compressible low-flow vessels

• CT:– Phleboli may be present secondary to

slow flow and intralesional thrombosis

• MR:– Hypo- to isointense on T1W

(heterogeneity may indicate hemorrhage or thrombosis)

– Hyperintense on T2W (low signal in areas of septation or thrombosis)

– Signal voids on T2W and GRE sequences secondary to phleboli

• TRICKS:– delayed enhancement of the venous

spaces and tortuous vessels with the absence of venous shunting

• Post TRICKS T1W with FS:– complete enhancement with the

exception of signal voids related to phleboli

Case 3: 15-year-old who presented with a left neck venous malformation

Sagittal T2 with fat saturation MR image demonstrates a hyperintense mass with multiple areas of low signal abnormality representing phleboli

Sagittal T1W with fat saturation post contrast MR reconstructed image demonstrates a centrally enhancing mass

Case 3: 15-year-old who presented with a left neck venous malformation 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 (AVMs)

• comprise 10% of all vascular malformations • often become symptomatic during puberty under the

influence of hormonal changes • marked clinically as pulsatile, warm areas of superficial

blushing • shunting may ultimately cause tissue ischemia, leading to pain

and ulceration of the skin

AVMs: Imaging• US:

– high-flow vessels with low arterial resistance and a higher venous peak velocity than other vascular malformations or hemangiomas

– arterialization of the draining veins with pulsatile flow

• MR:– Signal voids are typically present on

both T1W and T2W images with high-flow vessels demonstrating high signal on gradient echo

• TRICKS:– early enhancement with early venous

shunting through the nidus with good enhancement on first pass of the feeding arteries and dilated draining veins

– A steal phenomenon may be observed with preferential flow to the AVM, causing underdevelopment and atrophy of nearby musculoskeletal structures

• Post TRICKS T1 with FS:– enhancing vascularity but no defined

soft tissue mass

Case 4: 12 week old female with a right scapular AVM

Spectral color Doppler US image demonstrates a waveform typical for low arterial resistance with arterialization of the draining veins Coronal T1 with fat saturation post contrast MR image

demonstrate avid enhancement of the lesion

Case 4: 12 week old female with a right scapular AVMCoronal TRICKS MR image demonstrates the presence of early, dilated draining veins (arrows) which enhance in phase 7 of 15, concurrent with arterial vessels, indicating arteriovenous shunting

Lymphatic Malformations (LMs)

• Composed of chylous fluid, lined by endothelium • Further characterized as:

– Microcystic (cystic hygroma): numerous small cysts smaller than 2cm– Macrocystic (lymphangioma): larger cysts of varying size

• Most are present at birth with 90% seen at 2 years• Most common location is the head and neck with clinical

findings of rubbery and noncompressible

Lymphatic Malformations: Imaging• US:

– Microcystic: ill-defined and hyperechoic, due to the innumerable interfaces produced by the tiny cysts

– Macrocystic: multiloculated cystic lesions with vascular flow in the septa

• MR:– low signal on T1W and intense high

signal on T2W MR imaging due to fluid content

– increased T1 signal and fluid/fluid levels may be present due to proteinaceous or hemorrhagic content

– adjacent subcutaneous fat stranding may be present secondary to lymphedema

• TRICKS:– may show enlarged feeding vessels

or enhancement of septations– overwhelming majority and center of

the lesion will never enhance as opposed to hemangiomas

– no early venous drainage

• Post TRICKS T1 with FS:– Microcystic: typically no

enhancement– Macrocystic: only rim or septal

enhancement

Case 5: 10 week old female with a right chest wall macrocystic LM

Color Doppler US image demonstrates a complex cystic mass (arrows) with no internal vascular flow

Axial T1W with fat saturation post contrast images demonstrate a cystic mass with peripheral enhancement (arrows) suggestive of superimposed infection

Case 5: 10 week old female with a right chest wall macrocystic LMCoronal TRICKS MR image shows slightly enlarged intercostals arteries and peripheral enhancement of the lesion (arrow) in phase 11 of 35

Case 6: 22 year old female with a right arm low grade sarcoma

Coronal T1W with fat saturation post contrast MR images show an avidly enhancing soft tissue mass (arrow)

Magnified coronal oblique reconstructed image demonstrates findings suggestive of neovascularity of the lesion

Case 6: 22 year old female with a right arm low grade sarcoma Coronal TRICKS MR image 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

Case 7: 3-year-old who presented with neck bulging when crying with ectasia of the left

internal jugular vein

Axial double inversion recovery image demonstrates a dilated left internal jugular vein depicted as a flow void (arrow)

Case 7: 3-year-old who presented with neck bulging when crying with ectasia of the left internal jugular vein Coronal TRICKS MR image demonstrates enhancement of the left internal jugular vein (arrow) in phase 7 of 15

Conclusion

• Distinction between hemangiomas, vascular malformations and other vascularized tumors important as they are managed by different treatment regimens

• Time resolved contrast-enhanced MR Angiography has become an increasingly important adjunct in the diagnosis of vascular anomalies

• Optimization of the exam technique and familiarity of the TRICKS imaging appearance is essential and can often assist in accurate lesion characterization

References1. Mulliken JB, Glowacki J. Hemangiomas and vascular malformations in infants and children: a classification

beyond endothelial characteristics. Plastic and Reconstructive Surgery 1982; 69:412-4222. Burrows PE, Laor T, Paltiel H, Robertson RL. Diagnostic imaging in the evaluation of vascular birthmarks.

Dermatol Clin 1998; 16:455-4883. Dubois J, Alison M. Vascular anomalies: what a radiologist needs to know. Pediatr Radiol 2010; 40:895-9054. Moukaddam H, Pollak J, Haims AH. MRI characteristics and classification of peripheral vascular

malformations and tumors. Skeletal Radiol 2009; 38:535-5475. Swan JS, Carroll TJ, Kennell TW, et al. Time-resolved three-dimensional contrast-enhanced MR angiography

of the peripheral vessels. Radiology 2002; 225:43-526. Cornfield D, Mojibian H. Clinical uses of time-resolved imaging in the body and peripheral vascular system.

AJR 2009; 193:546-5477. Konez O, Burrows PE. Magnetic resonance of vascular anomalies. Magn Reson Imaging Clin N Am 2002;

10:363-3888. Herborn CU, Goyen M, Lauenstein TC, Debatin JF, Ruehm SG, Kroger K. Comprehensive time-resolved MRI of

peripheral vascular malformations. AJR 2003; 181:729-7359. Fayad LM, Hazirolan T, Bluemke D, Mitchell S. Vascular malformations in the extremities: emphasis on MR

imaging features that guide treatment options. Skeletal Radiol 2006; 35:127-13710. Sarkar M, Mulliken JB, Kozakewich HP, Robertson RL, Burrows PE. Thrombocytopenic coagulopathy

(Kasabach-Merritt phenomenon) is associated with Kaposiform hemangioendothelioma and not with common infantile hemangioma. Plast Reconstr Surg 1997; 100:1377-1386