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107

MR Imaging of Symptomatic Peripheral Vascular Malformations

Kevin M. Rak1 Wayne F. Yakes1’2 Robin L. Ra? James N. Dreisbach2 Steve H. Parker James M. Luethke1 A. Thomas Stavros2 Dick D. Slater1 Brian J. Burke1

We performed a retrospective study of symptomatic peripheral vascular malformations to determine if MR imaging can be used to distinguish slow-flow venous malformations from high-flow artenovenous malformations and arteriovenous fistulas. Twentyseven MR examinations in 25 patients with malformations outside the CNS were

reviewed.

Sixteen

venous

malformations,

nine arteriovenous

malformations,

and

two

were included. In all cases, the MR findings were correlated with the results of angiography. The distinction between slow-flow venous malformations and high-flow arteriovenous malformations and artenovenous fistulas was made primanly on T2-weighted MR images, which showed high signal intensity in venous malformations and flow voids in high-flow lesions. In addition to the previously described MR features of venous malformations (serpentine pattern with septations, associated muscle atrophy, and typical TI and T2 signal intensities), several new MR features were apparent. Venous malformations had a propensity for multifocal involvement (37%), artenovenous

orientation

fistulas

along

the

long

axis

of extremities

or affected

muscles

(78%),

and

adherence

to neurovascular distributions (64%). Prominent subcutaneous fat was commonly seen adjacent to the malformation. MR images of arteriovenous malformations and artenovenous fistulas also commonly showed muscle atrophy and subcutaneous fatty prominence. Our results show that slow-flow venous malformations can be distinguished from high-flow artenovenous malformations and fistulas on the basis of spin-echo MR signal characteristics. The associated imaging characteristics help in the differential diagnosis in problematic

AJR

cases.

159:107-112,

July 1992

Symptomatic vascular malformations include venous malformations, arteriovenous malformations (AVM5), arteriovenous fistulas (AVF5), and mixed lesions. Historically, angiography and venography have provided the most specific diagnostic information, but MR has recently been shown to be useful in evaluating these Received April 5, 1991 ; accepted February 4, 1992.

after revision

The opinions and assertions contained herein are the privateviews of the authors and are not to be construed as official or as reflecting the views of the Department Defense. 1

Department

Medical

Center,

reprintrequests 2

Medical

Center,

of the Army

or Department

of Radiology, Aurora,

Fitzsimons

CO 80045-5001.

to K. M. Rak. Imaging Associates, Englewood,

Army Address

P. C., Swedish

CO 80110.

0361-803X/92/1591-0107 © American Roentgen Ray Society

of

lesions [1 -7].

MR depicts

the anatomic

relationships

between

vascular

malforma-

tions and adjacent organs, nerves, tendons, and muscles, thereby providing significant help in therapeutic planning, be it surgical or ethanol endosurgical ablation [8-13]. The goals of the study were twofold: (1) to evaluate the usefulness of MR in

distinguishing slow-flow lesions (venous malformations) from (AVMs and AVF5) and (2) to describe additional MR features

high-flow of these

malformations

before

that,

lished. Twenty-seven malformations

were correlated findings in 16.

were

with

to the best

of our knowledge,

MR examinations reviewed.

CNS

arteriographic

have

in 25 patients lesions

findings

were

not

never

with symptomatic included.

in all cases

lesions various

been

pub-

peripheral

The

MR findings

and with

venographic

108

RAK ET AL.

Materials

and Methods

wise

Over a 20-month period, 25 patients (1 5 females, 10 males) 8-63 years old (mean, 23 years) were referred to our institutions for

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evaluation

and treatment

of vascular

malformations

outside

the CNS.

Sixteen venous malformations were studied: three in the extremity, two in the face or neck, and 1 1 in the lower extremity

upper

(two extended into the pelvis or buttocks). Nine AVMs were three in the pelvis, two in the face or neck, two in the paraspinal region, one in the lower extremity, and one in the upper extremity. Both AVFs studied were in the lower extremity: one was of which evaluated:

a single

congenital

AVF

and

the

other

numerous posttraumatic AVFs. Twenty-seven MR examinations separate

vascular

malformations

was

in a patient

were performed; in anatomically

who

had

two patients had unrelated

regions,

necessitating two angiographic and MR studies in each of these patients. Equipment included 1 .5-T Signa (General Electric, Milwaukee, WI), O.5-T Vista (Picker International, Highland Heights, OH), and 0.5-T Magnetom (Siemens, Iselin, NJ) imaging systems. In all but one of the examinations, were

used.

Each

at least

two

was

imaged

lesion

orthogonal with

planes

spin-echo

relative

each of the 1 4 venous

malformations

localized ography, by using criteria,

to an extremity was studied by using closed-system yenand two face and neck venous malformations were studied direct puncture venography. On the basis of angiographic the lesions were categorized as venous malformations, AVMs, or AVFs. Venous malformations were characterized arteriographically as having normal inflow arteries, a normal intervening capillary bed, and contrast pooling in dilated stagnant venous spaces in the late venous phase. AVMs were characterized arteriographically as having

enlarged

inflow

arteries

with

draining veins. No intervening capillary

prompt

bed

shunting was

an intervening

capillary

bed,

but

usually

have

a single

arteriovenous connection [1 31. At our institutions, ethanol embolotherapy is the primary means of treatment for symptomatic vascular malformations;

therefore,

surgical

correlation

in all

cases

was

not

possible. However, in seven of the patients with venous malformations, biopsy was performed: in each case the histologic findings corresponded to the MR and angiographic interpretations. The MR images were interpreted retrospectively by three radiologists who had full knowledge of the angiographic findings. The MR and angiographic studies were interpreted together, in hopes of delineating additional imaging characteristics that would make it possible to distinguish low-flow from high-flow vascular malformations, and expanding on differential diagnostic features. Subsequently, once the MR criteria were established for distinguishing

venous malformations from AVMs and AVFs, all 27 MR examinations were reanalyzed by two other radiologists. These radiologists categorized

the

lesions

on the

but were otherwise blinded, results or clinical data.

basis

of our previously

having

described

no knowledge

criteria,

of angiographic

Ti

Each vascular malformation was evaluated by using biplane selecIn addition,

lack

July 1992

of acquisition (SE)

weighting, 500-i 000/i 5-20 (TR range/TE range), and more T2 weighting (1 500-2500/20-90). Gradient-echo(GRE)sequences were obtained in i 8 cases: 1 3 by using a single-slice technique, 20-50/ 1 1-1 5/i 0-30#{176} (TR/TE/flip angle), and five by using a multiplanar technique (500-1 000/20-30/i 0-30#{176}). tive arteriography.

AJR:159,

present.

into tortuous

AVFs like-

Results Of the 16 venous malformations evaluated, all had similar MR signal characteristics: predominantly decreased signal intensity compared with fat on Ti -weighted images, hyperintense signal compared with fat on T2-weighted images, and increased signal intensity compared with skeletal muscle on both Ti and T2-weighted images (Fig. 1). With Ti weighting, scattered small foci of higher signal intensity, comparable to -

the intensity

of fat, were

commonly

noted.

GRE images

in 10

lesions corresponded to long TR/TE SE sequences, with increased signal found in the abnormal vascular elements of the venous malformation. Low-signal linear striations were uniformly seen within the lesions with both SE and GRE sequences.

Fig. 1.-Typical MR characteristics of slow-flow venous malformation

forearm

in

of I 1-year-old boy.

A, Ti-weighted

SE (600/20)

coronal

MR image shows that involved area has signal

intensity

slightly

higher

than that

of skeletal muscle but less than that of subcutaneous fat. Areas of higher Ti signal intensity may be related to fatty replacement (arrows). B, T2-welghted SE (2000/80) coronal

MR image shows higher signal intensity of venous malformation relative to muscia and subcutaneous fat. C, Corresponding closed-system yenogram shows extent of lesion is better defined with MR than with venography,

because of incomplete fication

of lesion.

contrast opaci-

MR OF PERIPHERAL

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AJR:159, July 1992

with arteriography.

Also, note involvement

i 09

MALFORMATIONS

Fig. 3.-Asymmetric fatty prominence associated with venous malformation in a 47-yearold man. T2-weighted (2000/80) axial MR image of thighs shows normal left thigh and asymmetric prominence of subcutaneous fat (curved arrows) associated with venous malformation (straight arrows) in anterior subcutaneous fat of right thigh.

Fig. 2.-Multifocal venous malformation in a 23-year-old man. T2-weighted (2200/90) axial MR image shows anatomically separate focus in soft palate/uvula (arrows) that was

not detected

VASCULAR

of

left gingiva.

In five of the 16 cases, fatty infiltration or replacement in the involved or adjacent musculature was present. In no case

was a prominent feeding artery or draining vein detected. In three cases, phleboliths were detected; these correlated with calcifications

seen

on plain films.

larger than typical

linear striations

In four

cases,

signal

voids

were seen within the vascular elements and no corresponding phleboliths were detected on plain films. Thirteen of the i 6 lesions had muscular or fascial

involvement,

whereas

solely to the subcutaneous i 3 lesions with muscular

three

lesions

were

fat. On MR imaging, or fascial involvement

infiltration of the associated tendons. One lesion intramedullary component within the femur, as noted

MR and arteriography.

In six of the i 6 venous

smaller, secondary sites shown to be anatomically

We determined

limited

two of the also had had an on both

malformations,

of involvement were detected and separate from the primary focus.

that these venous

malformations

were multi-

focal in distribution (Fig. 2). Of the five venous malformations in which images of the contralateral extremity were available, hypertrophic subcutaneous fat was present on the affected

side in four cases (Fig. 3). Eleven of the i 4 venous malformations in the extremities were oriented along the long axis of the extremity, paralleling fascial planes (Fig. 4). Of these i 4 lesions, nine followed an identifiable neurovascular distribution (two along the radial distribution,

two

along

the sciatic distribution [i 4], two along tibial distribution, two along the posterior tibial

the anterior distribution, and one along the peroneal distribution). The adjacent vascular distributions were not involved (Fig. 4). In nine of the i i high-flow

and was SB). She and

vascular

malformations

(AVM5

AVF5) imaged, the main MR feature on SE sequences the presence of flow-related signal voids (Figs. 5A and An exception was in a patient with a paraspinal AVM. had MR imaging after several unsuccessful operations subsequent radiation therapy. These previous treatments

Fig. 4.-Ancillary

characteristics

a 21-year-old woman. A, Ti-weighted (600/20)

malformation to peroneal partments.

coronal

of venous malformation MR image

shows

along long axis of right lower extremity

in right calf of

orientation

of venous

and strict adherence

venous distribution, sparing anterior and posterior Subcutaneous fat is also asymmetrically prominent

tibial cornalong me-

dial aspect of affected limb. B, corresponding closed-system malformation to peroneal venous

were

thought

to account

venogram distribution.

shows

for the lesion’s

adherence

atypical

of venous

MR appear-

ance: small central flow voids and a larger surrounding of fibrous scar. In another patient, metallic artifacts surgical

clips

obscured

visualization

of an arteriovenous

area from fis-

RAK ET AL.

110

AJR:159,

July 1992

Fig. 5.-Typical MR characteristics of a high-flow lesion in a 50-year-old man with pelvic arteriovenous malformation. A, Ti-weighted

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SE (600/20) coronal MR Image shows prominent flow voids in nidus (white arrows) of arteriovenous malformation, and tortuous feedlag artery (straight black arrow) and dilated draining vein (curved arrow) proximal to nidus. B, T2-weighted (2500/80) axial MR image shows persistence of flow voids (arrows) within malformation.

C, Corresponding gradient-echo (50/13/20#{176}) axial MR image shows high signal intensity within areas of void on SE images, indicating that areas are flow related. 0, Corresponding subtraction anglogram, arterlographic phase, shows enlarged arterial feeders (black arrows) and large vascular nidus (white arrows).

tulous connection. In each of the remaining nine patients with AVMs or AVFs with no previous surgical intervention, prominent flow voids were seen on Ti and T2-weighted SE sequences. By contrast, in the eight patients in whom GRE images were obtained, these areas had higher signal intensity (Fig. 5C). Arteriographic correlation was provided in all cases (Fig. 50). The single-slice and multiplanar GRE techniques were not used concurrently; thus, a direct comparison of these techniques was not possible. In seven of the 1 1 patients with AVMs or AVFs, dilated -

feeding arteries and draining veins, commonly tortuous, detected proximal to the abnormal vascular connections

were

(Fig. 5A). Other than by following the larger inflow and outflow vessels to their site of origin or drainage, SE or GRE sequences could not be used to accurately distinguish the smaller

arteries

from

veins.

Although

phase

imaging

was

not

used, this technique might be able to provide this information. Of four patients with AVMs or AVFs in the extremities, two had fatty infiltration of adjacent musculature. In nine patients with

AVMs

or AVFs

in whom

the contralateral

also imaged, six had asymmetric neous faton the affected side.

prominence

extremity

was

of subcuta-

On the basis of these MR characteristics (T2 signal intensity, presence or absence of dilated feeding arteries or draining veins, orientation, multifocality), 26 of the 27 vascular malformations

were

correctly

characterized

by the

second

(blinded) group of the radiologists as being low flow or high flow. The only error was in the paraspinal AVM, which was atypical in appearance, presumably as a result of the patient’s previous

treatment.

Discussion Symptomatic vascular malformations make up a spectrum of vascular anomalies. Venous malformations are postcapillary dilated venous spaces typified by stagnant flow, lack of normal venous valves, and absence of arteriovenous shunting. They have commonly been referred to in the literature as hemangiomas.

However,

on the basis of differences

in cellular

characteristics, endothelial hyperplasia and regression, and clinical behavior, we concur with the work of Mulliken at al. Li 5-i 7] and believe that hemangiomas of infancy and venous malformations

are separate

and distinct

vascular

anomalies.

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MR OF PERIPHERAL

July 1992

AJR:159,

VASCULAR

MALFORMATIONS

iii

Further, unlike venous malformations, on MR imaging, hemangiomas consistently have high-flow signal voids within the lesion. This has been observed by us and by others [7].

of associated single AVFs mations. In one of these

AVMs are also congenital lesions with arteriovenous shunting without an intervening capillary bed. AVFs may be congenital

sity on the GRE images. We postulate, on the basis of these findings, that the presence of concurrent AVFs, although not common, might occasionally account for these atypical areas of signal void within venous malformations on SE imaging. The multifocal nature of venous malformations, occurring in 37% of the patients in our series, is important information for planning treatment of these vascular malformations. The results of surgical treatment of venous malformations have historically been disappointing [6, 20]. With incomplete resection, the residual malformation becomes aggressive and

obtained,

or posttraumatic and also have high-flow shunting similar to that of AVMs. In contrast to AVMs, usually only a single arteriovenous communication is present in AVFs. However, in a long-standing posttraumatic AVF, neovascular recruitment of multiple arteries can simulate an AVM near the

arteriovenous connection [1 8, i 9]. Our results show that slow-flow venous consistently

be distinguished

from

AVFs on the basis of MR findings. tions

had predominantly

malformations

the high-flow

All 1 6 venous

high signal

intensity

can

AVMs

and

malforma-

SE sequences. In contrast, all AVMs and AVFs that had not been treated before MR imaging had mainly signal voids on all SE sequences. These flow voids are attributed to both time-of-flight phenomena and turbulence-related dephasing. On MR imaging, venous malformations have a character-

istic serpentine and associated

commonly

The complete known before

frequently

area had higher signal inten-

more so than it was preoperatively.

extent of the vascular malformation any treatment is initiated [8, 1 0,

will show the full extent

must be 1 3]. MR

of the malformation

more

accurately than can be achieved by using the combination of arteriography and venography (Fig. i). Furthermore, as many

venous malformations are multifocal, MR can be used to guide the angiographic evaluation of unsuspected areas of adjacent involvement, and to depict anatomic relationships to

pattern with internal striations and septations focal muscle atrophy. The described signal

intensity is greater than that of skeletal muscle on both Ti and T2-weighted images, but less than that of subcutaneous fat on Ti sequences and greater than that of fat on T2 sequences. Pathologically, these findings have been correlated with fibrofatty septa between endothelium-lined vascular channels. The high signal intensity seen on SE sequences with long TR/TE has been attributed to stagnant flow in these abnormal vascular spaces [2, 3, 5]. Newly described MR characteristics in our patients include a propensity for discontinuous multifocal involvement, a tendency for orientation

and the corresponding

symptomatic,

on long TR/TE

in two of the 1 6 venous malfortwo cases, GRE images were

-

aid in therapeutic

malformation uvula were

planning.

noted

The abnormal malformation

In one patient

(Fig. 2), secondary

with a facial

on MR and not detected

postcapillary are better

venous

foci in the soft palate

vascular

opacified

with

spaces

with

and

arteriography.

of a venous

closed-system

venog-

raphy than with arteriography. In anatomic sites such as the face and neck, in which closed-system venography is difficult to perform, MR can show sites of involvement not detected by standard arteriography with delayed venous-phase imaging. Although it is not a substitute for venography, MR may

along the long axis of affected extremities, a tendency to follow neurovascular distributions, occasional extension into tendon sheaths, and associated enlargement of adjacent

be useful in localizing the site for direct-puncture The addition of GRE sequences in imaging formations is not essential, but it does increase

subcutaneous

of findings, particularly for high-flow lesions. Areas of signal void on SE sequences are not specific for flow, but are confirmed to be flow related by high signal intensity with GRE images (Fig. 5). However, the low-flow and high-flow lesions

tissue dysplasia

fat. This

suggests

a more

rather than a dysplasia

diffuse

isolated

congenital

to the mal-

formed vascular spaces. Orientation along the long axis of the extremity, multifocality, and absence of dilated feeding

arteries

or draining

in differentiating

veins are additional low-flow

from

characteristics

high-flow

shared by low-flow and high-flow include associated muscle atrophy prominence. Although not uniformly

lesions.

helpful Features

vascular malformations and subcutaneous fatty seen, these characteris-

tics may be helpful in distinguishing vascular malformations from other soft-tissue masses. One caveat for our study is that only symptomatic malformations were evaluated (i.e., patients requiring therapy). As such, asymptomatic or less

extensive vascular malformations might not have characteristics exactly like those we have described. Four of the 16 venous malformations had areas of signal void larger than those associated with typical linear septations, but these mation (making

were only a minor component of the malforup only a small proportion of the lesion) as

compared with being the dominantfeature in AVMs and AVFs. Previously cited explanations for these areas of signal void in venous malformations on SE sequences are thrombosed vessels, phleboliths, and linear, fibrous striations cut in cross section

[S]. In our series,

angiography

showed

the presence

venography. vascular malthe specificity

are not as readily differentiated on GRE images, because of the higher signal of each when flow-sensitive techniques are used. In conclusion, we have documented the ability of MR to consistently distinguish slow-flow venous malformations from

high-flow verified

AVMs

or AVFs

the typical

MR

and have described differential diagnosis.

with

SE MR imaging.

features

new

findings

of vascular

that

We have

malformations,

should

aid in their

REFERENCES 1 . Levine E, Wetzel LH, Neff JR. MR imaging and CT of extrahepatic cavernous hemangiomas. AJR 1986;147: 1299-1304 2. Yuk WTC, Kathol MH, Sein MA, Ehara S, Chiu L. Hemangiomas of skeletal muscle: MR findings in five patients. AJR 1987:149:765-768 3. Buetow PC, Kransdorf MJ, Moser RP, Jelinek JS, Berrey BH. Radiologic appearance of intramuscular AJR i990;154:563-567

hemangioma

with emphasis

4. Cohen JM, Weinreb JC, Redman HC. Arteriovenous

on MR imaging.

malformations

of the

112

RAK ET AL.

extremities:

5. Cohen

MR imaging.

EK, Kressel

hemangiomas:

correlation

1079-1 081 6. Pearce WH, Rutherford

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Radiology

HY, Perosio with

1986;158:475-479

T, et al. MR imaging pathologic

RB, Whitehill

findings.

of soft AiR

tissue 1988;150:

TA, Davis K. Nuclear

magnetic

resonance imaging: its diagnostic value in patients with congenital malformations of the limbs. J Vasc Surg i988;8:64-70 7. Meyer JS, Hoffer FA, Barnes PD, Mulliken JB. Biological classification of soft-tissue

vascular

anomalies:

MR correlation.

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8. Yakes WF, Haas KD, Parker SH, et al. Symptomatic

vascular malforma-

tions: ethanol embolotherapy. Radiology i989;170: 1059-1066 9. Yakes WF, Luethke JM, Parker SH, et al. Ethanol embolization of vascular malformations. RadioGraphics i990;10:787-796 10. Yakes WF, Parker SH, Gibson MD, Haas DK, Pesner PH, Carter TE. Alcohol embolotherapy of vascular malformations. Semin Intervent Radio! 1989:6: 146-1 61 11. Yakes WF, Luethke JM, Merland JJ, et al.Ethanol embolization of arteriovenous fistulas: a primary mode of therapy. J Vasc Intervent Radio! i990;1 :89-96 12. Yakes WF, Pesner P, Reed M, Donohue HJ, Ghaed N. Serial embolizations of an extremity arteriovenous malformation with alcohol via direct percutaneous puncture.AJR 1986:146:1038-1040

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13. Yakes WF, Parker SH. Diagnosis and management of vascular anomalies. In: Castaneda-Zuniga WR, Tadavarthy SM, eds. Interventional radiology, 2nd ed. Philadelphia: Williams & Wilkins, 1991 : 152-1 89 14. McLeIIan GL, Morettin LB. Persistent sciatic artery: clinical, surgical and angiographic aspects. Arch Surg 1982:117:817-822 15. Mulliken JB, Glowacki J. Hemangiomas and vascular malformations in infants and children: Plast Reconstr Surg

a classification

based

on endothelial

characteristics.

1982:69:412-420 16. Upton J, Mulliken JB, Murray JE. Classification and rationale for management of vascular anomalies in the upper extremity. J Hand Surg i985;6:970-975 17. Finn MC, Glowacki J, Mulliken JB. Congenital vascular lesions: clinical application of a new classification. J Pediatr Surg i983;18:894-900 18. Lawdahl RB, Routh WD, Vitek JJ, McDowel HA, Groww GM, Keller PS. Chronic arteriovenous fistulas tions: diagnostic considerations

masquerading as arteriovenous and therapeutic implications.

malformaRadiology

1989;170:1011-1015 19. Trout HH, Tievsky AL, Rieth KG, Drug EM, Giordano JM. Arteriovenous fistula simulatingartenovenous malformation. Otolaryngol Head Neck Surg 1987:97:322-325

20. Szilagy DE, Smith RF, Elliot JP, Hageman JH. Congenital anomalies of the limbs. Arch Surg 1976;111:423-429

arteriovenous

Roentgen Ray Society Award Papers, 1993

The ARRS announces competition for the 1993 President’s Award concerning the clinical application of the radiologic sciences.

and two Executive

Council

Awards

for the best

papers

Awards The winner of the President’s Award will receive a certificate and a $2000 prize. The winners of the two Executive Awards will each be given a certificate and a prize of $i 000. The winners will be announced on March 15, i 993. Winning papers will be presented at the ARRS annual meeting at the San Francisco Marriott, San Francisco, CA, April 25-30, 1993. Winning papers will be submitted for early publication in the American Journal of Roentgenology. All other papers will be returned to the authors. Council

Regulations Eligibility radiologic manuscript.

is limited discipline.

to residents A letter

from

or fellows the

in radiology

who have not yet completed

4 years of approved

training

resident’s department chairman attesting to this status must accompany must be the sole or senior author and be responsible for all or most of the project.

in a the

The resident Submitted manuscripts must not exceed 5000 words and have no more than 10 illustrations. Four copies of the manuscript and illustrations are required. Submitted manuscripts should not contain previously presented or published material and should not be under consideration for publication elsewhere. Deadline for submissions is February 12, 1993. Send papers to Nancy 0. Whitley, M.D. Chairman, Committee on Education & Research American Roentgen Ray Society Department of Radiology University of Maryland Medical Systems Hospital 22 S. Greene St. Baltimore, MD 21 20i