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    28 APPLIED RADIOLOGY www.appliedradiology.com April 2010

    There has been increasing reliance

    on computed tomography angi-

    ography (CTA) and magnetic

    resonance angiography (MRA) for eval-

    uation of the intracranial vasculature inpatients suspected of acute stroke. Digi-

    tal subtraction angiography (DSA),

    while traditionally the gold standard, is

    invasive and associated with potential

    complications. Further, DSA is not read-

    ily accessible anytime day or night. In

    the acute stroke setting, DSA is typically

    reserved for patients undergoing thera-

    peutic intervention with intra-arterial

    thrombolysis or embolectomy.

    The purpose of this article is to com-

    pare the diagnostic accuracy of CTA,

    MRA and DSA for evaluation of the

    intracranial circulation in patients with

    stroke. We will discuss the technical

    parameters and potential artifacts that

    must be understood so that an accurate

    interpretation of each modality can be

    made. We will structure our discussion

    around an illustrative clinical case of a

    patient who underwent CTA, MRA and

    DSA within a 24 hour time frame.

    Clinical case

    A 62-year-old man presented to theemergency room with acute onset

    diplopia, diffuse weakness and vomit-

    ing. Given the concern for posterior-

    circulation ischemia, a CT/CTA was

    requested and performed within the first

    hour of symptom onset (Figure 1). Ourstandard CT stroke protocol included

    64-slice CTA from the base of the heart

    through the cerebral vertex, as well as

    delayed contrast-enhanced head CT

    obtained approximately 1 min after CTA

    (without the need for additional contrast

    material because contrast has already

    been injected for CTA). In this patient,

    the initial CTA demonstrated lack of

    opacification of the bilateral distal verte-

    bral arteries and proximal basilar artery,

    while the delayed contrast-enhanced

    images demonstrated normal opacifica-

    tion of the left distal vertebral artery and

    proximal basilar artery.

    Based on the clinical and imaging

    findings, the patient received IV tissue

    plasminogen activator (tPA) and

    underwent 3-dimensional time of flight

    (TOF) intracranial MRA approxi-

    mately 4 hours following CTA to

    reassess his vasculature after throm-

    bolysis (Figure 2). The MRA demon-

    strated absence of flow-related

    enhancement in the bilateral distal ver-tebral and entire basilar artery, which

    was discrepant with the initial CTA,

    especially considering that there was

    no change in the patients clinical

    examination and no evidence of neuro-

    logic deterioration between initial CTA

    and follow-up MRA.

    The patient then underwent DSA the

    following day, approximately 24 hours

    after the initial CTA, to reevaluate his

    vasculature (Figure 3). Again, there

    was no neurologic deterioration at the

    time of the study. DSA demonstrated

    occlusion of the right vertebral artery,occlusion of the left vertebral artery

    proximal to the posterior inferior cere-

    bellar artery (PICA), reconstitution of

    the vertebrobasilar confluence distal to

    the PICA, and occlusion of the remain-

    der of the basilar artery with filling of

    the basilar tip via the posterior commu-

    nicating artery.

    The important point about this case is

    that CTA, contrast-enhanced CT, MRA

    and DSA obtained within 24 hours of

    each other, and without any change in

    the patients clinical status, demon-

    strated very different findings. Both

    MRA and DSA appeared to demon-

    strate occlusion of the basilar artery, as

    well as occlusion of the bilateral distal

    vertebral arteries. However, most of the

    basilar artery appeared patent on CTA,

    which showed occlusion limited to the

    bilateral distal vertebral arteries and

    only the most proximal aspect of the

    basilar artery. Delayed contrast-

    enhanced CT, in turn, appeared to

    demonstrate patency of the distal leftvertebral and entire basilar artery.

    One explanation for the discrepancy

    is that the patients basilar artery

    thrombosed between the time of CTA

    and MRA/DSA. However, the absence

    of any neurological changes between

    examinations, as would be expected

    with a typically devastating basilar

    artery occlusion, weighs against this

    Intracranial vascular imaging:Pearls and pitfalls

    Jane J. Kim, MD, and Max Wintermark, MD

    Dr. Kim is Assistant Professor of Clini-cal Radiology, Neuroradiology Section,San Francisco General Hospital, Uni-versity of California, San Francisco, CA;andDr. Wintermarkis Chief of the Divi-sion of Neuroradiology, University ofVirginia Health System, Charlottesville,VA.

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    possibility. A more likely explanation for

    the radiologic discrepancies lies in each

    imaging modalitys way of capturing andassessing vascular flow.

    Accurately reading intracranial CTA,

    MRA and DSA to avoid pitfalls of inter-

    pretation requires an understanding of the

    technical parameters and potential arti-

    facts underlying eachmodality.

    CT angiography

    The steady introduction of CT scanners

    with ever - increas ing numbers

    of detector rows has enabled greatercraniocaudal coverage at increasingly

    faster scan times and better resolution.

    Current state-of-the-art clinical stroke

    CTA imaging relies on 64-slice CT, which

    can scan from the aortic arch through the

    intracranial vessels in a matter of 3 to 4 sec

    at submillimeter isotropic resolution.

    Acquisition time is significantly shorter

    than single-slice CTA and 4-slice CTA.

    This also means that less contrast material

    is used and that contrast material has less

    time to circulate within the vessels on 64-

    slice CTA than on s ingle- or 4-s l iceCTA.

    The entire duration of 64-slice CTA,

    from start of contrast injection to con-

    clusion of scanning, is approximately 20

    to 25 sec. Because image acquisition only

    requires 3 to 4 sec, most of this time is due

    to the delay between when contrast is

    injected and when scanning is begun.

    This 15 to 20 sec delay is necessary to

    ensure optimal opacif ication of the

    cervical and intracranial vessels, and the

    precise amount of delay can be deter-

    mined by either timing bolus or by a bolus-tracking technique.13 We use the former

    in our stroke CTA protocol.

    The contrast-enhanced head CT that is

    obtained after 64-slice CTA in our stroke

    protocol utilizes contrast material that was

    previously injected for the CTA, and does

    not require that any additional contrast be

    used. Contrast-enhanced CT is obtained

    approximately 60 sec after CTA, which

    a l lows addi t iona l t ime for contras t

    material to circulate within the body as

    compared with 64-sl ice CTA. In our

    clinical example, CTA showed lack of

    opacification of the distal left vertebral and

    proximal basilar artery, both of which

    appeared opacified on delayed contrast-

    enhanced CT; only the distal right ver-

    tebral artery appeared occluded on both

    CTA and delayed CT. It is likely that slow or

    low f low through the d is ta l le f t and

    proximal basilar artery caused them to

    appear occluded on fast 64-slice CTA,

    while delayed contrast-enhanced CT

    allowed for greater contrast circulation to

    establish patency. Figure 4illustrat es a similar case in a different

    patient.

    These cases show that areas of sig-

    nificantly delayed blood flow, secondary

    to proximal vessel stenosis or distal

    thrombosis, may be imaged by rapid 64-

    slice CTA before adequate contrast

    opacification has occurred. The scan can

    30 APPLIED RADIOLOGY www.appliedradiology.com April 2010

    INTRACRANIAL VASCULAR IMAGING

    FIGURE 1. 62-year-old man with acute

    diplopia, weakness and vomiting. Axial source

    images from computed tomography angiogra-

    phy (CTA) demonstrated no opacification and

    apparent occlusion of bilateral distal vertebral

    arteries (A) and very proximal basilar artery(B). The remainder of the basilar artery

    demonstrated robust opacification (C) on

    coronal reformatted images from CTA. Axial,

    delayed contrast-enhanced CT (obtained

    1 min after CTA) showed opacification of the

    left distal vertebral artery (D) and proximal

    basilar artery (E), both of which appeared

    occluded on the initial CTA.

    A B

    C D

    E

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    www.appliedradiology.com APPLIED RADIOLOGY 31April 2010

    outrun the contrast material circulation

    in areas of slow flow, which are able to

    opacify by the time delayed contrast-

    enhanced CT is ob ta ined . Ar te r ia l

    pseudo-occlusion is a type of flow artifactincurred by fast CT scanning.

    CTA is reported to have high sensitivity

    and spec if ic i ty for de tec t ion of

    intracranial stenoses and occlusions. Two

    recent studies indicated high sensitivity

    and specificit y of CTA for detecting

    moderate/severe stenosis (>97%); for

    occlusion, the sensitivity and specificity

    were even h igher (approaching

    100%).4,5 The positive predictive value of

    CTA for diagnosing intracranial occlu-

    sion was 100% in these studies. Both of

    these studies evaluated images obtainedon ear l ie r -genera t ion CT scanners

    (single- and 4-slice in one study, 8- and 16-

    slice in the other). The longer image-

    acquisition time in these studies may help

    to explain the lack of any false-positive

    findings of occlusion. However, with

    increased availability and adoption of

    very fast CT scanning with 64-slice

    scanners , the poss ib i l i ty of image

    acquisition outrunning the contrast bolus

    in cases of slow or altered flow should be

    considered to prevent overestimating and

    misdiagnosing occlusion.

    MR angiographyPublished literature on 3-dimensional

    intracranial TOF MRA shows equivalent,

    to slightly lower, sensitivity of MRA as

    compared with CTA for diagnosis of steno-

    occlusive disease. Sensitivity ranges

    between 70% to 100% for detecting

    moderate/severe stenosis, and between

    87% to 100% for occlusion; specificity is

    close to 100% forboth.4,6,7

    However, MRA has several importantlimitations. Unlike CTA and DSA, which

    employ a contrast agent to directly image

    the blood within a vessel, TOF MRA relies

    on the magnetization of spins flowing into

    an imaging slice and is prone to certain flow

    artifacts.

    TOF MRA uses a grad ien t echo

    sequence and a rap id success ion of

    INTRACRANIAL VASCULAR IMAGING

    FIGURE 2. 3-Dimensional time of flight magnetic resonance angiography (MRA, A) obtained

    on the same patient (4 hours after CTA and IV tissue plasminogen activator [tPA] treatment)

    demonstrated absence of flow-related enhancement in the bilateral distal vertebral and entire

    basilar artery. Compare this with findings on the initial CTA (B), which showed opacification of

    the basilar artery. The patient did not have any change in neurological exam between initial

    CTA and follow-up MRA.

    FIGURE 3. Digital subtrction angiography (DSA) on the same patient after thrombolysis with

    IV tPA and approximately 24 hours after initial CTA. Right vertebral artery injection, AP view

    (A), showed occlusion of the distal right vertebral artery (arrow) and no opacification of the

    basilar artery. Left vertebral artery injection, AP view (B), showed similar occlusion of the distal

    left vertebral artery (black arrow) proximal to the posterior inferior cerebellar artery (PICA)

    (white arrow). Left vertebral artery injection, lateral view (C), again demonstrated distal verte-

    bral artery occlusion (black arrow), reconstitution of the vertebrobasilar confluence (arrow-

    head) distal to PICA (white arrow), and occlusion of remainder of the basilar artery. Internal

    carotid artery injection, lateral view (D), showed filling of the basilar tip (arrow) via the posterior

    communicating artery. However, most of the basilar artery appeared occluded. This did not

    change on late arterial and venous phases (not shown).

    A B

    A B

    C D

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    32 APPLIED RADIOLOGY www.appliedradiology.com April 2010

    radiofrequency (RF) pulses to saturate

    and suppress s ignal f rom stationary

    background t is sue . Blood s i tua ted

    outside the imaging plane remains rel-

    atively unaffected by the pulses and flowsinto the imaging plane with magneti-

    zation intact, generating br ight MR

    signal (flow-related enhancement). As

    such, ideal TOF imaging requires that

    background tissue be completely sup-

    pressed, and that inflowing blood be

    completely unsaturated to generate

    maximal s igna l . This is no t a lways

    achievable in practice.

    Background may not be entirely sup-

    pressed with tissues that have short T1

    relaxation times, such as fat, hematoma or

    thrombus. These tissues quickly recovertheir longitudinal magnetization despite

    the rapid succession of RF pulses, and are

    able to generate bright MR signal that may

    interfere with image interpretation and

    obscurearteries.

    Flowing blood may also experience

    saturation effects by RF pulses. Slow

    flowing blood spends more time within a

    given imaging volume, making it sus-

    ceptible to saturation by RF pulses. Areas

    of slow flow due to proximal or distal

    stenosis/thrombosis may have signal

    loss and appear occluded.

    Areas of turbulent blood flow near a

    stenosis can also appear occluded due to

    signal loss. The observation of signal loss

    due to spin dephasing at stenoses with

    turbulent flow has been described in both

    phantom models and clinical studies.6,8,9

    Finally, re trograde f low through

    collateral vessels (in cases of vessel

    occlusion) may not be depicted. TOF

    imaging frequently uses a saturation band

    to suppress all flow-related enhancement

    opposite in direction to arterial flow,which typically eliminates unwanted

    venous s ignal but may also have the

    unintended consequence of suppressing

    retrograde collateral flow. Knowledge of

    these potential pitfalls is critical for

    accurate interpretation of MRA. This is

    espec ia l ly re levant to acu te s t roke

    imaging , as pa t ien ts wi th ce rebra l

    INTRACRANIAL VASCULAR IMAGING

    FIGURE 4. 79-year-old woman with acute left hemiparesis. CTA shows apparent occlusion of

    the entire right internal carotid artery (ICA) from its origin in the neck to the carotid terminus,

    including at the skull base (A) and cavernous portion (B). Delayed contrast-enhanced images

    (C,D), however, demonstrate opacification and patency of the right ICA at comparable levels.

    DSA performed 4 hours after CTA confirms patency of the entire right cervical ICA (E) and

    intracranial ICA (F). There is an abrupt occlusion of the proximal right M1 segment of the mid-

    dle cerebral artery (black arrow, F). No other stenoses or occlusions were seen on the right,

    and nonopacification of the r ight ICA on CTA was attributed to slow flow resulting from distal

    M1 occlusion.

    A B

    C D

    E F

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    34 APPLIED RADIOLOGY www.appliedradiology.com April 2010

    INTRACRANIAL VASCULAR IMAGING

    thromboembolic disease are more likely

    to have alterations in flow dynamics with

    slow flow, turbulent flow and retrograde

    flow.

    Given the potential for artifactualsignal loss with TOF MRA in cases of

    altered flow, it is not surprising that MRA

    has a high false-positive rate for detection

    of intracranial stenosis and occlusion.

    Bash et al. compared CTA, MRA and

    DSA findings in patients suspected of

    acute cerebrovascular events, and found

    that MRA had positive predictive values

    of 65% for stenosis and 59% for occlu-

    sion, compared with 93% and 100% for

    CTA.4

    In our clinical example, the basilar

    ar tery appeared pa tent on CTA butoccluded on MRA obtained 4 hours later,

    following thrombolysis. It is likely that the

    distal vertebral artery occlusion resulted in

    slow flow through the basilar artery and/or

    re t rograde f low through pos te r ior

    communicating arteries, causing arti-

    factual signal loss on MRA. The complete

    absence of any clinical deteriorati on

    between CTA and MRA makes basilar

    artery occlusion unlikely. MRA in this case

    was falsely positive for occlusion, a

    conclusion that can be reached given an

    understanding of flow artifacts common

    toTOF MRA.

    Digital subtraction angiographyDSA is tradition ally considered the

    gold s tandard for assessment of the

    in tracran ia l vascula ture , and is the

    modali ty with which CTA and MRA are

    compared. In our clinical case, DSA

    showed occlusion of most of the basilar

    artery, with only minimal opacification

    of the vertebrobasilar confluence and

    basilar tip (the latter via posterior com-municating arteries on carotid injection).

    However, CTA and delayed contrast-

    enhanced CT had previously shown good

    opacificati on of the basilar artery and

    there had been no interval change in the

    patients clinical status between CT and

    DSA.

    Given the CT f ind ings and s tab le

    clinical examination, it is likely that DSAreflected a false-positive finding of

    basilar ar tery occlusion. Bash et a l .

    reported cases of false-positive DSA

    findings of occlusion in 6 of 28 patients

    (21%) who presented with symptoms of

    acute stroke and underwent CTA, MRA

    and DSA.4All 6 cases involved the pos-

    terior circulation and occurred in very

    slow- or low-flow states distal to a sig-

    nificant stenosis, causing the vessel to

    appear occluded on DSA but stenotic (and

    otherwise opacified) on CTA. MRA was

    also falsely positive for occlusion in 4 ofthese 6 cases. The conclusion of a false-

    positive DSA finding was reached by

    consensus re-evaluation of the data in all 6

    cases.

    The likely explanation for the dis-

    crepancy between CTA and DSA findings

    in our case, as well as the reported cases, lies

    in differences in image acquisition time.

    Angiographic runs are typically obtained

    over 5 sec (at a 4 frames-per-second film

    rate) and capture a single intracranial

    circulation cycle. A single intracranial

    circulation cycle, from opacification of the

    carotid siphon to maximal opacification of

    the cortical veins, lasts approximately 4 to 6

    sec.10,11 While 64-slice CTA is extremely

    fast, time from contrast injection to scan

    completion is 20 to 25 sec and still leaves

    more time for contrast material to circulate

    through areas of severe stenosis than on

    DSA. Delayed contrast-enhanced CT

    obtained 60 sec after CTA allows even

    more time for contrast material circulation

    to opacify patent segments of the vessel

    lumen on either side of stenotic or occludedareas.

    ConclusionOur clinical case and l iterature review

    highlights several important points about

    intracranial vascular imaging with CTA,

    MRA and DSA. C TA and MRA have

    fairly high sensitivity/specificity for

    detection of intracranial stenoses andocclusions, when using DSA as the gold

    standard. However, flow-related arti-

    facts can create the appearance of vas-

    culature occlusion in each modality. The

    mechanism by which th is occurs is

    different.

    In TOF MRA, signal loss can occur due

    to slow, turbulent or retrograde flow; this

    is well known and described extensively

    in the literature. In contrast, flow-related

    artifacts are not typically associated with

    CTA or DSA. As acquis i t i on t imes

    become increas ingly shor te r wi thgreaterdetector-row CT scanners, the

    possibility of image acquisition out-

    running the contrast bolus and producing

    pseudo-occlusion must be considered.

    Knowledge of these potential pitfalls is

    usefu l and may prevent inaccura te

    in te rpre ta t ion of imaging f ind ings

    caused by dynamic alterations to blood

    flow in patients with cerebrovascular

    disease.

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