1. Montefiore Medical Center
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 Center
Bronx, NY

2. 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

3. 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

4. Mulliken and Glowacki Classification
Hemangiomas
Vascular Malformations
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
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

5. 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

6. 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

7. 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

8. 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

9. Our Technique
3 month old with a left chest wall hemangioma
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)

10. 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)

11. 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

12. 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

13. 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

14. Typical 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 FS*
Axial T2 with FS
TRICKS
TR/TE (msec)
475/20
4000/102
425/17
5.9/2
Flip angle (degrees) - 20 45
Section thickness (mm) 3 5
1.6
NEX 2
0.5
Matrix
224 x 256
192 x 256
256 x 320
FOV (mm)
variable
15-24
480
No. of sections
24-30
40-50
30-40
Imaging time (sec)
300
240 / 270 (with FS)
360
/ (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

15. 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:
Determination of avid, early arterial enhancement or minimal to moderate arterial enhancement on T1W FS post contrast images
TRICKS temporal enhancement pattern
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

16. Algorithm Minimal to Moderate Enhancement Avid Enhancement
T1W with FS post TRICKS Enhancement
Minimal to Moderate Enhancement
Avid Enhancement
Central Enhancement
Peripheral Enhancement
TRICKS Enhancement Pattern
Early Arterial Enhancement
Late Arterial/Venous Enhancement
Presence of dilated veins
Rim Type
Heterogeneous and septated
Presence of early dilated draining veins
Not definitely a vascular malformation
Yes No
Venous Malformation
Macrocystic LM
Microcystic LM vs. Tumor with Hemorrhage
AVM
Hemangioma

17. 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

18. Hemangiomas: Imaging US: MR: TRICKS: Post TRICKS T1W with FS:
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

19. 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

20. 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

21. 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

22. 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

23. 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

24. Case 2: 3 month old female with thrombocytopenia and leg swelling with a KHE
Coronal 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)

25. 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

26. Venous Malformations: Imaging
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

27. 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

28. 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)

29. 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

30. AVMs: Imaging US: MR: TRICKS: Post TRICKS T1 with FS:
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

31. 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

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

33. 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

34. 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

35. 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

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

37. Case 6: 22 year old female with a right arm low grade sarcoma
Magnified coronal oblique reconstructed image demonstrates findings suggestive of neovascularity of the lesion
Coronal T1W with fat saturation post contrast MR images show an avidly enhancing soft tissue mass (arrow)

38. 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

39. 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)

40. 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

41. 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

42. References
Mulliken JB, Glowacki J. Hemangiomas and vascular malformations in infants and children: a classification beyond endothelial characteristics. Plastic and Reconstructive Surgery 1982; 69:
Burrows PE, Laor T, Paltiel H, Robertson RL. Diagnostic imaging in the evaluation of vascular birthmarks. Dermatol Clin 1998; 16:
Dubois J, Alison M. Vascular anomalies: what a radiologist needs to know. Pediatr Radiol 2010; 40:
Moukaddam H, Pollak J, Haims AH. MRI characteristics and classification of peripheral vascular malformations and tumors. Skeletal Radiol 2009; 38:
Swan JS, Carroll TJ, Kennell TW, et al. Time-resolved three-dimensional contrast-enhanced MR angiography of the peripheral vessels. Radiology 2002; 225:43-52
Cornfield D, Mojibian H. Clinical uses of time-resolved imaging in the body and peripheral vascular system. AJR 2009; 193:
Konez O, Burrows PE. Magnetic resonance of vascular anomalies. Magn Reson Imaging Clin N Am 2002; 10:
Herborn CU, Goyen M, Lauenstein TC, Debatin JF, Ruehm SG, Kroger K. Comprehensive time-resolved MRI of peripheral vascular malformations. AJR 2003; 181:
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:
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: