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Traumatic vertebral artery injury: a review of the screening criteria, imaging spectrum, mimics, and pitfalls

Purpose Traumatic vertebral artery injury (TVAI) can have a varied clinical presentation and appearance on imaging. In this review, we present the screening criteria, spectrum of imaging features, grading, and imaging pitfalls of TVAI. Our review focuses on the imaging of TVAI on computed tomography angiography (CTA), magnetic resonance angiography (MRA), and cases of TVAI mimics. Imaging The imaging spectrum on CTA can range from either focal or long segment luminal stenosis (the most common findings), smooth or tapered narrowing of lumen, string of pearls appearance, concentric intramural haematoma, intimal flap (the most definite sign), and double lumen of the artery. On time-of-flight MRA, the most common findings include loss of flow void within the vessel due to slow flow, thrombosis or occlusion, and hyperintense signal within the vessel wall due to intramural haematoma on T1 fat-saturated images. Conclusion The reader should be aware of the screening criteria, common and uncommon findings, variant anatomy, artifacts, and mimics of TVAI when evaluating cases of craniocervical trauma, to be competent in calling in or ruling out injury.


Introduction
Traumatic vertebral artery injuries (TVAI) should be sus pected clinically in the setting of cervical spine trauma with symptoms of neck pain and/or vertebrobasilar ischae mia. Blunt cerebrovascular injury (BCVI) is the umbrella term used for traumatic vascular injuries of the head and neck arteries; however, we have limited the scope of this article to imaging of TVAI.
The major reasoning for early detection of BCVI is to prevent the possibility of stroke, which can occur in 1013% cases, resulting in potential permanent neurologi cal deficits [1]. With early detection of BCVI, the incidence of stroke can be reduced to as low as 0.5% by initiation of appropriate treatment, which can include antithrombot ic medications or vascular intervention versus untreated BCVI, in which the incidence of stroke can reach 21% [2].
The clinical scenarios for both BCVI and TVAI are similar. There have been several grading systems and screening criteria set up for detection of BCVI, includ ing the Denver [3], Memphis [4], and Boston [5], cri teria based on injury mechanism, injury pattern, and symptoms. The initial screening criteria were set up in the 1990s [6] and were further expanded by the Denver group in 2005 [3]. This modified Denver criteria is the most widely used criteria in practice [1]. More recent lite rature from 2011 proposed expanding screening criteria to detect asymptomatic earlystage BCVI in order to further reduce the risk of stroke [7]. Application of this expanded screening criteria has improved detection of BCVI from 2.3 to 2.9% [8] (Table 1 depicts the expanded screening criteria for detection of BCVI proposed in 2011 by Burlew et al. [7]).
However, a balance has to be struck between excess imaging and not missing out on asymptomatic vascular injury. Use of expanded screening criteria or ordering CT angiography (CTA) for all cervical spine fractures can lead to a higher false negative rate. The decision to use either conservative classic screening criteria or more expanded screening criteria remains controversial and an area of ongoing research. However, there remains no doubt that angiographic imaging is mandated for detecting vascular injury in cases of complex cervical spine fractures, sub luxations, fractures involving facet joints, or the transverse foramina (covered under the modified Denver criteria), which tend to have a high incidence of concomitant vas cular injury and higher yield of vascular injury cases [9]. However, the caveat remains that utilising limited screen ing criteria can miss up to 20% of cases. In conclusion, the decision regarding the optimal screening criteria will have to be made by an institution based on its available resourc es and local standards of care.

Imaging modalities for detection of traumatic vertebral artery injuries
Digital subtraction angiography (DSA) has historically been considered the gold standard for diagnosis of vas cular injury in the head and neck. But DSA is an invasive test, which may not be readily available at smaller hospi tals. An invasive test also makes it a less favourable option to be used as a screening tool. DSA is also limited to the evaluation of the vessel lumen and can miss out on detect ing cases with nonstenotic intramural haematoma [10]. The role of DSA for diagnosis now would be limited to evaluating highrisk patients who have equivocal or neg ative results on CTA [11]. Now with improvements in CT technology, CTA has proven to be the initial screening test of choice in head and neck vascular imaging. CTA has recently shown remark ably improved detection of BCVI, especially with 64slice and higher CT scanners [12]. In one study, CTA demon strated a high sensitivity of close to 98% and specificity close to 100%, when compared to DSA [13]. How ever, achieving these high numbers requires that the radio logists are able to sustain the quality of reading by being more familiar with the spectrum of imaging in BCVI and TVAI, which is the aim and scope of this article.
Doppler Duplex US has a very limited problemsolv ing role. It cannot be used for screening due to its poor sensitivity because large portions of the vertebral arteries are not accessible for sonographic detection. Hence, its sensitivity for TVAI is even lower than for detection of ca rotid injuries [14]. The advantages of doppler US, howev er, are its safety, availability, and ability to detect direction of flow in the vertebral arteries.
Magnetic resonance angiography (MRA) plays a com plementary role when combined with MRI for concom itant detection of strokes with MRI and vascular injury with MRA. However, when judged by its ability to detect vascular injury, it is less sensitive compared to either CTA or DSA. Studies have found low sensitivities for MRA for detection of TVAI in the range of 4760% [4]. We present a brief overview of normal and variant anatomy of the vertebral arteries. We follow that with a pictorial review of the imaging spectrum of TVAI in cluding grading of the injury along with the mimics and pitfalls to be aware of.

Normal anatomy
The vertebral artery (VA), in most people, are paired struc tures arising from the first part of the subclavian arteries. It then ascends posterior to internal carotid artery, oblique ly superiorly and medially towards the cervical spine. Either at the C6 or C7 level, it enters the foramen transversarium/ transverse foramen, which is an aperture within the transverse processes of the cervical vertebrae. It ascends through the foramen transversaria till C2. The transverse foramina con tain VA, vertebral veins, and sympathetic plexus. From C2, the VA sweeps laterally to pass through the transverse fora men of C1 and passes superiorly to pierce the dura and arach noid to extend intracranially and then joins the contralateral VA to form the basilar artery. Anatomical landmarks have been utilised to divide the vertebral artery into segmentsthe V1 (extraosseous segment) from origin to entry into its caudal most transverse foramen, V2 (foraminal segment or pars transversaria) -typically from C6 to C2 within the trans verse foramina, V3 (extraspinal segment or atlas loop) from C2 to dura at the skull base, and V4 (intradural intracranial segment) from dura to confluence ( Figure 1).

Variant anatomy
The VA may arise directly from the brachiocephalic arteries or directly from the aortic arch instead of the subclavian artery. The VA may be asymmetric in size with one vessel being dominant. The left VA is more commonly dominant. The finding of VA hypoplasia, although a developmental variant, has been reported to have a higher incidence of VA dissection and posterior circulation stroke [15]. It can sometimes be difficult to conclude whether smaller size of the VA is due to developmental hypoplasia or due to ac quired stenosis. Hypoplasia is usually a diffuse finding and the entire VA is diffusely small calibre. However, there may be, on occasions, an isolated narrow V4 segment after the origin of the posterior inferior cerebellar artery or even the V4 segment terminating as the posterior inferior cerebel lar artery [16]. These should not be mistaken for stenosis or TVAI. A useful clue for developmental hypoplasia is that the size of the transverse foramen in also small with a developmentally small VA. Stenoses tend to occur seg mentally whereas hypoplasia is a diffuse finding. Dupli cation and fenestration of the vertebral arteries and of the vertebrabasilar junction is also a rare variant [17,18]. This should be identified as a variant and not mistaken for the twovessel sign of TVAI.

Mechanism and grades of traumatic vertebral artery injuries
The mechanism of TVAI usually involves both preex isting intrinsic susceptibility and a precipitating event. Although a normal VA can undergo injury from major trauma, minor trauma can also cause TVAI when there is an underlying arteriopathy, which may be congenital or genetic, like connective tissue disorders, fibromuscular dysplasia, or vessel wall weakening caused by infection or inflammation of the vessel wall. Pathological evaluation of cases of spontaneous cervical artery dissections have found changes of Ehlers Danlos syndrome and Marfan syndrome in the vessel wall [19]. This, superimposed with a minor or major trauma, leads to intimal tears, which are the subtlest form of injury. These tears can be seen as thin intimal flaps on imaging in the vessel lu men. This dissection can progress further when luminal blood enters through the intimal defect and extravasates in the vessel wall creating a false lumen. The false lumen can extend for a variable length and can remain patent or more frequently thrombose due to slower flow. More severe injury can manifest when the vessel wall ruptures, and a pseudoaneurysm may be formed if the rent in the vessel wall is small. In most severe forms of injury, the vessel may become occluded or transacted, which is usu ally fatal [2022].
On review of the literature, the predominant aetiolo gy was found to be highvelocity motor vehiclerelated injuries; however, other cause like a fall, sporting acci dent, chiropractic manipulation, and hanging, although less common, have been described [9]. Distractive flexion injury is the main mechanism for TVAI, instead of the hyperextension injury as previously thought [23,24].

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Location of TVAI: Most TVAI are located in the V2 or V3 segment [25,26]. The V2 segment is the most common ly affected in adult TVAI. In infants and children, the V3 and upper V2 segment are more commonly affected [27].
The grading of TVAI severity proposed by the Denver group is the most widely used and is depicted in Table 2 [9]. We subsequently present examples of these grades in the imaging spectrum that follows.

Imaging spectrum Computed tomography angiography
Technique: CT angiography (CTA) of head and neck, when performed with modern 64slice or higher CT scan ner, provides thinslice (1 mm or less), highresolution imaging of the arterial lumen and the wall of the VA. Bolus tracking of the contrast is incorporated in the pro tocol in order to obtain optimal phase of maximum opaci fication of the arteries. Modern CT scanners are faster at scanning as well limiting late contrast bolus and artefacts from thicker slices associated with older CT scanners. Generation of multiplanar coronal and sagittal recon structions, MIP (maximum intensity projection), and VR (volume rendered) imaging are among the common pro tocols for CT angiographic imaging, and these multiple views and projections help to establish a more confident assessment of the anatomy and pathology.
CTA Findings of TVAI: The findings on CTA will vary as per the grade of injury. The commonly encountered imaging findings of TVAI on CTA are smooth tapered luminal narrowing, concentric or focal luminal narrow ing of the VA ( Figure 2AC), or total occlusion (Figure 3), with these findings seen in more than 50% cases. Other findings seen are, double lumen ( Figure 4A), intimal flap (Figure 4BG), dilatation of artery ( Figure 4FH), beaded appearance of artery or string of pearls appearance (Fig  ure 4IK) or stenosis of lumen. The most definite sign is double lumen or intimal flap, which is not frequently seen (in around 22% cases), and the most common imaging characteristic is nonspecific luminal stenosis (seen in more than 50% cases) [28]. CTA can show contrast extravasation or pseudoaneurysm formation, which are signs of more severe injury ( Figure 5).
CTA Pitfalls: The CTA images may be affected by poor bolus timing, bone, dental, or metallic artefacts in the spine or from patient's motion, swallowing, or pulsation artefacts, which limit image interpretation. Poor bolus may show contrast in arteries and veins simultaneously, giving the appearance of two lumens. Tortuosity of the vessel may also give the false appearance of two lumens. Atheroscle  This is an issue with evaluation in older patients who have preexisting atherosclerotic changes in their vessels. Arte rial wall thickening or diminished flow due to severe ste nosis may cause false positive interpretation for TVAI [29]. Developmentally hypoplastic VA can mimic long segment arterial injury, but usually can be ascertained by a smaller ipsilateral transverse foraminal diameter ( Figure 6). An other limitation is that CTA is not a dynamic study, so it is difficult to interpret if there is retrograde filling of the affected vertebral artery or reversal of flow. Refer to Table  3 for a summary of the TVAI CTA findings and pitfalls. Care should be taken while calling in a TVAI because there could be other medical conditions that can lead to similar findings of occlusion or stenosis. The patient's clin ical history should be kept in mind. The most common mimickers are fibromuscular dysplasia, atherosclerosis, and postradiation treatment changes.

Magnetic resonance angiography and magnetic resonance imaging
Technique: TVAI can be assessed with MRA either with or without contrast. The ability to image without contrast is especially helpful in patients with contraindications to iodinated contrast material. The imaging protocol for noncontrast MRA includes either 2D or 3D timeof flight imaging, which detects the velocity of flowing pro tons. Another technique is phase contrast imaging, which can provide quantitative estimation of the flow velocity. T1 images of the neck with fat saturation are also per formed as part of standard protocol because the blood in the false lumen -the intramural haematoma -appears hyperintense in the subacute phase ( Figure 7). Usage of gadolinium contrast is optional, but it does improve the imaging of the lumen of the arteries secondary to opaci fication by T1 relaxation effects of gadolinium. MRI of the brain can be performed at the same time as the MRA. The MRI, especially diffusion sequence, can help detect the presence of acute infarction, for which it is exquisitely sensitive and specific when compared to CT. Other fac tors that affect the imaging characteristics are the field strength of the scanner, patient body habitus, the signal intensity from the surrounding structures, and the imag ing sequence protocol used [30,31].

Magnetic resonance angiography findings of traumatic vertebral artery injuries
The intramural haematoma in the false lumen after dissec tion is hyperintense on T1weighted images in subacute

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stages between seven days and two months and is detected on the fatsaturated imaging. Subacute haematoma is seen as crescentic hyperintense areas around an eccentric flow void [30,32]. However, it is isointense in acute or chronic stages (within six months). When the haematoma is isoin tense, as in acute or chronic dissections, it becomes tough to detect. Other findings seen on MRA are loss of flow void or occlusion ( Figure 8AB), similar to what can be seen on CTA. The 3D TOF technique is better than the 2D TOF in regard to spatial resolution, but it increases the scan time. Contrast MRA has greater ability to evaluate the lumen, especially for subtle luminal irregularities and stenosis [32,33]. MRA Pitfalls: The false positives on MRA are due to turbulent flow producing hyperintense signal in the pe riphery with central flow void simulating stenosis or in tramural haematoma ( Figure 8CD). Additionally, periar terial structures like fat or veins can simulate intramural haematoma or pseudoaneurysm ( Figure 8EF). These are more confounding when there is developmental asymme try in the size of the VA ( Figure 8F). Comparison with other sequences, fat saturation, or CT images may be help ful in such cases [29,34]. Entry slice phenomenon causing a bright signal in the artery at the extreme of the imaging volume due to entry of unsaturated spin can simulate an intramural abnormal signal or the absence of an expect ed flow void simulating dissection. Also, the flowrelated enhancement in the veins adjacent to VA can simulate in tramural haematoma or dissection on unenhanced MRA (TOF). These can be overcome by the application of satu ration pulses cranially and caudally to the imaging volume [29,35]. V1 segment VA dissection may be missed with V1 inadvertently not included in the image volume, and small dissection may be missed due to gaps in image slabs [31]. In early or acute stages, the intramural haematoma may be isointense on T1weighted images, in such cases other signs may be helpful, like luminal narrowing or pseudoan eurysm formation. In subacute stages, the bright intramu ral haematoma may be masked by the background bright signal from fat or indistinguishable from the flowrelated enhancement on MRA. The bright signal from an occlud ed vessel may obscure the bright intramural haematoma; however, this can be resolved by contrastenhanced MRA with subtraction of unenhanced images [29]. Asymmetry in the size of the VA may be mistaken for dissection in a smaller lumen artery ( Figure 8F). Careful observation of the periarterial bright signal on TOF, only seen in dissec tion rather than normal artery, should be performed [34]. Comparing the luminal diameter on the VA above and below the site of injury can help in calling in or ruling out normal asymmetry with confidence. In contrastenhanced MRA there might be segmental blurring of the signal in   VA due to rapid circulation times, especially in young pa tients, called the feathering artefact, and it may simulate small stenosis. This can be overcome by using an earlier trigger time with elliptical centric contrast enhanced MRA [33]. MR is also limited in the detection of pseudoaneu rysms because they are mostly seen at the skull base with abnormal flow or signal within and may mimic a mass le sion [34,36]. Refer to Table 4 for a summary of the TVAI MRA findings and pitfalls.

Digital subtraction angiography
DSA, although traditionally considered a gold standard, is limited by lack of ability to assess the arterial wall con figuration and thickness. The common signs seen on DSA are: complete occlusion of lumen (Figure 9), "string sign", and "string and pearl sign", which refers to long tapered eccentric irregular stenosis without or with distal dila tation. Pathognomonic signs, such as intimal flap and or double lumen, are rarely observed [37]. When there is a ta pered occlusion, it is referred to as the "Flame Sign" [38]. The major advantage of DSA is that it is a dynamic acqui sition. Hence it does not suffer as much from contrast ki netics and bolus timing as CTA. Hence, DSA is sometimes performed to supplement evaluation in indeterminate cases, assess the collateral circulation, or rarely as part of endovas cular repair. If there is good collateral circulation, patients usually do well with conservative management (Figure 10).

Doppler duplex ultrasound
US doppler duplex imaging has limited sensitivity in detecting mainly extracranial VA dissection. Distal V2 and V3 segments cannot be adequately evaluated due to a poor acoustic window. However, there are some features that are beneficial, like rapid mobility, costef fectiveness, and noninvasiveness, but it is not sensitive enough to exclude intimal tears [39]. Hence, it is not suit ed to initial evaluation of a trauma patient when injury needs to be ruled out. However, it can be useful as a prob lemsolving tool. The ability to easily detect direction of flow in the vertebral artery is also helpful when compared to CTA and MRA. Spectral imaging with peak systolic velocity values and waveform morphology helps estimate the presence of stenosis. If TVAI can be visualised accu rately, then it has a role for followup of vertebral artery dissection [40].

Management and treatment
TVAIs are usually managed conservatively with either anti coagulation or antiplatelet therapy. The used anticoagulant medications include warfarin and heparin. Used antiplate let agents include aspirin, clopidogrel, and dipyridamole. The optimal regimen with respect to agent, duration of treatment, or end point of therapy is not known. Often the associated injuries limit antithrombotic therapy. In such cases, endovascular interventions are another ther apeutic option [41]. Grade I and II injuries are managed conservatively with medical management. Anticoagu lation, typically with heparin, acutely followed by three months of warfarin was the traditional management. In 2015, the Cervical Artery Dissection in Stroke Study trial (CADISS) suggested no difference in efficacy of antiplatelet and antithrombotic agents in preventing stroke and deaths in patients with symptomatic vertebral artery dissection [42]. This may encourage wider use of antiplatelet agents over anticoagulation agents considering the better safety profile of the former with respect to haemorrhagic compli cations. For grade III injuries with pseudoaneurysm, the initial treatment again is antithrombotic therapy. However, if the size of the pseudoaneurysm reaches from 11.5 cm or is symptomatic then endovascular stenting or coiling may be performed [41,43]. For grade IV injuries with arterial thrombosis, the initial treatment is with antithrombotic therapy, and treatment outcomes with endovascular ther apy are not known yet. Grade V injuries are mostly fatal, and surgical exploration is recommended if possible.

Conclusions
Imaging with CTA is the initial test of choice in patients with trauma, who meet the screening criteria for the pos sibility of cervical vascular injury. MRA, DSA, and Dop pler duplex US have complementary secondary roles in imaging. Early detection is key because initiation of ther apy can dramatically reduce the incidence of associated strokes. Familiarity with the key findings of TVAI, ana tomic variations, mimics, and pitfalls depicted and sum marised in this review should assist the readers in more accurate estimation of TVAI.