Management of Blunt Cerebrovascular Injury: A Literature Review

Abstract

Blunt cerebrovascular injury (BCVI) is one of the most common clinical manifestations in patients with skull base trauma and severe traumatic brain injury. It is also the cause of later stroke, including ischemia and hemorrhage. Screening high-risk patients by several grading scales will support the identification and management of the complications of BCVI. Computerized tomographic angiography (CTA) and digital subtraction angiography (DSA) play a crucial role in identifying the lesion of cerebrovascular injuries. Antithrombotic therapy is the essential treatment for minimizing the risk of BCVI-related. This chapter aims to review the updated management of BCVI.

1. Introduction

Blunt cerebrovascular injury includes blunt macrovascular and penetrating cerebrovascular injuries, which occur in about 1% of all traumatic brain injuries, 9% in severe traumatic brain injuries, and 1–2% in the in-hospital trauma population. Most of the lesions are found in the extracranial segment of carotid and/or vertebral arteries.

Patients with cervical spine trauma, including upper cervical spine, ligamentous injuries, and traumatic subluxation placing, have the strongest association with BCVI. However, the LeFort II or III fracture and basilar skull fracture extending carotid canal patients should be alerted to BCVI. These lesions are most commonly identified in trauma patients with high-energy injury mechanisms, for example, car accidents, falling… with flexion, extension, or rotation of the neck, or a direct blow to or laceration of the blood vessels. Blunt carotid injury generally causes contralateral hemiparesis or hemiplegia, aphasia, dysphasia, or Horner syndrome. Ataxia, dizziness, or visual field deficits can be resulted from blunt vertebral injury.

The imaging modality for diagnostic BCVI still focuses on CT angiography and DSA. The standard of reference is DSA, but CT angiography becomes popular and contributes many useful characteristics of BCVI. All patients with high-risk factors for BCVI should undergo DSA as the final test for BCVI.

While the application of screening protocols is accepted generously, the treatment remains a discussion. Early identification and treatment of BCVI help reduce the rate of mortality and morbidity. Antithrombotic therapy, either with anticoagulation or antiplatelet agents, has long been accepted as the first-line of BCVI patients. However, the medication choice and the duration of treatment are still controversial.

2. Epidemiology

The prevalence of BCVI as a variant depends on the different studies. A systematic review and meta-analysis from Franz et al. [1], the incidence range of BCVI was between 0.18 and 2.7% among 122.176 blunt trauma patients. This result came from 20 studies published from 2004 to 2011.

Another prospective, observational, single-center study published in 2016 showed the incidence of BCVI was 9.2% among 228 patients with severe traumatic brain injury. The three most common risk factors included motorcycle crash, fracture involving the carotid canal and cervical spine injury [2].

The study by Hundersmarck et al. [3] showed that 0.59% of BCVI patients in 12.122 blunt trauma populations. The most popular mechanism of trauma in Hundersmarck’s research was a car accident (31%) followed by fail from stairs (24%). Motor vehicle collision or other modes of transportation is also the most frequent reason of BCVI (56.1%) in a total of 1.204 patients during 10-year follow-up at a level I trauma center [4]. The result of this study showed about 42% BCVI population suffered from traumatic brain injury. The highest incidence of BCVI met in patients with cervical trauma (7.3%), followed by basilar skull fracture (1.6%), polytrauma (1.5%), and whole blunt trauma group (0.59%).

A study by Wu et al. [4] collected 1204 BCVI patients (2.5%) in a group of 47.773 blunt trauma patients. CT angiography is the key imaging to confirm the vessel injuries. The incidence of BCVI-related stroke in this research was 8.5%, the median time to stroke was 2 days (with a range of 0–12 days).

Another study by Esnault et al. [2] found that BCVI accounts for 9.2% of all severe traumatic brain injury admissions. These included 71% with carotid artery injury, 24% with vertebral artery injury, and 5% with damage to both.

The injury of carotid artery and vertebral artery in the study of Harper et al. [5] were 47 and 58%, respectively. But the difference in the incidence of stroke between internal carotid (8.8)% and vertebral injuries (3.6%) was not statistically significant.

3. Mechanisms of BCVI

High-energy injury mechanisms are confirmed as the cause of BCVI by many researchers [2, 6, 7, 8]. High-speed motor vehicle collisions are the most popular cause of BCVI, but chiropractic manipulation, direct blows to the neck, and any mechanism resulting in rapid deceleration or acceleration accompanied with or without rapid head turning was reported as the cause of BCVI. Esnault et al. [2] categorized the main mechanism of BCVI: hyperextension with contralateral rotation of the head, laceration of the artery by adjacent fractures, direct blow to the neck, and direct intraoral trauma with a hard object. This categorization is similar to the opinions of Crissey and Bernstein in 1974. These two authors introduced 4 physiologic mechanisms which include direct blow to the neck, hyperextension with contralateral rotation of the head, laceration of the artery by adjacent fractures involving the sphenoid or petrous bone, and direct intraoral trauma with a hard device. Traumatic brain injury and skull base fractures can make easily a carotid artery injury, whereas cervical spine injury is associated with vertebral artery lesions. The most common mechanism of carotid artery injury is hyperextension caused by stretching of this artery over the lateral processes of C1 to C3.

4. BCVI screening

Some guidelines are recommended for screening patients who had high risk of BCVI, including Denver criteria and/or modified Denver criteria [9], Western Trauma Association (WTA) [7] screening recommendation, and Eastern Association for the Surgery of Trauma (EAST) [10]. The summary of screening recommendations for BCVI is shown in the Table 1.

Signs/symptoms

Massive hemorrhage from the neck, nose, and mouth,; Cervical hematomas develop.; Cervical bruit in a patient below 50 years old; Focal neurological deficit; Appearance of the secondary stroke on CT or MRI

Risk factors for BCVI

Maxillofacial fractures from high-energy mechanism, including mandible fracture, Le Fort II or III fractures.; Complex skull, basilar skull and/or occipital condyle fractures.; Cervical spine fracture or subluxation, including vertebral body fracture, transverse foramen fracture, subluxation or ligamentous injury, any fracture at C1 through C3.; Severe traumatic brain injury; Traumatic brain injury with thoracic injuries

Table 1.

Signs, symptoms and risk factors of BCVI.

Research by Biffl et al. [11] identified independent risk factors for BCVI after the follow-up of 249 patients by CT angiography. These included GCS less than 6, petrous bone fracture, diffuse axonal brain injury, and Le Fort II or III fracture. The high-risk mechanism patient with one of these circumstances was associated with a 41% risk of BCVI. The result of this study also announced that a patient with a cervical spine fracture had a 39% risk of vertebral arterial injury.

Screening for BCVI was recommended as level II by EAST in case of unexplained neurologic symptoms or arterial epistaxis after the traumatic brain injury. This guideline also gives a recommendation with III level for the asymptomatic patients who suffered from traumatic brain injury with Glasgow Coma Scale less than or equal to 8, a diffuse axonal injury, petrous bone fracture, fracture at high cervical segments [10]. The advantage of applying a screening tool helps the detection of BCVI increase versus no screening protocol [12].

A new screening model created by Japanese neurosurgeons was published in 2021 [13]. A multivariate analysis indicated 13 factors that were significantly associated with BCVI. These elements were sex (male – female), high-energy impact, hypotension on admission, Glasgow Coma Scale score below 9, injury to the face, injury to the neck, injury to the spine, injury to the lower extremity, supratentorial subdural hemorrhage, skull base fracture, cervical spine fracture or subluxation, lumbar spine fracture or subluxation, soft tissue injury of the face. When the definition of BCVI was narrowed to include only carotid and vertebral artery injuries, the AUC of the model in predicting these injuries was 0.89 (95%CI, 0.87–0.91).

5. Imaging

5.1 Digital subtraction angiography (DSA)

DSA plays a key role and standard imaging modality for the diagnosis of BCVI, but it still has some limitations. This method is an invasive, cost-effective tool, has a complication rate of 1–3% which includes vascular dissection and thromboembolism, and not provide by all trauma centers as a full-time, 24/7 service. With the development of CTA, DSA is mostly performed when an intervention is planned.

According to EAST guidelines [10], DSA was given a level II recommendation in screening BCVI. The two latest systematic review and meta-analysis study of CTA versus DSA in BCVI diagnosis suggests that CTA has reasonable specificity but low sensitivity [14, 15]. The pooled sensitivity and specificity of CTA were 64% (95%CI, 53–74%) and 95% (95%CI, 87–99%), respectively when compared to DSA. This guideline showed the estimated positive likelihood ratio, a negative likelihood ratio, and a diagnostic odds ratio was 11.8 (95%, 5.6–24.9), 0.38 (95%, 0.30–0.49), and 31 (95%, 17–56), respectively [15]. To determine the accuracy of CTA versus DSA in evaluate the lesions between BCVI carotid and BCVI vertebral, the result showed the similar in sensitivity and specificity.

5.2 CT angiography

Most of the patients who had BCVI got the polytrauma presentation. The BCVI candidates always have an indication for screening whole-body for prevention of the missing-lesions such as thoracic, abdomen, and spine. Hundersmarck et al. [3] indicated an augmentation of the dose of intravenous contrast administration flow for total body CT scanning from 3 to 6 ml/s to advance the diagnostic yield for cervical vascular lesions. Because of this remodeling, an increase in explorer incidence from 0.3 to 0.8%, from 0.9 to 2.4%, from 1.2 to 1.9%, from 4.6 to 8.5% in the whole blunt trauma group, in the polytrauma subgroup, in patients with a basilar skull fracture and in the cervical spine trauma subgroup, respectively, have been shown. These authors believe that in the setting of not scanning the total body, the patients may benefit from the modification for confirming the grade of cervical artery injuries. CTA can be used to classify and follow-up BCVIs. It can provide important decisions in the management and planning of the treatment of lesions.

In a European level 1 trauma center, the incidence of BCVI was changing between period I (using 64-slides scanner) and period II (using 256-slides scanner) [3]. During the first period, BCVI incidence was found to be 0.3% in the whole blunt trauma patients, 0.9% in the polytrauma subgroup, 1.2% in patients with basilar skull fracture, and 4.6% in the cervical spine trauma subgroup. With 256-slides scanner, the result in an increase of detected was 0.8% in the whole blunt trauma group, 2,4% in the polytrauma population, 1.9% patients with basilar fractures, and 8.5% cervical spine trauma subgroup.

CTA is a useful modality for the purpose of follow-up the BCVI patients. Wu et al. [4] suggest that CTA has the highest diagnostic yield in identifying the changing of lesions within the first 30 days after the trauma. These authors also confirm the best effect on the treatment of BCVI when CTA was performed within 30 days of injury. However, CTA has intermediate effects between 30 and 90 days, and no transformation when performed beyond 90 days, particularly in high-grade injuries.

However, the difference of channel CTA can affect the result. One- to four-slice multidetector CT angiography is neither sensitive nor specific enough for screening BCVI, and a minimum 16-channel CT angiography is available sensitive technology for diagnosis BCVI [6, 8, 10]. Kik et al. [15] showed the sensitivity and specificity that were reported at 70.3% (95%CI, 41.3–88.9) and 96.1% (95%CI, 86.5–98.9) in over 16-slice group, respectively, and 63.1% (95%CI, 46.3–77.2) 94.6% (95%CI, 61.0–99.5) in below 16-slice-CTA group, respectively. The systematic review and meta-analysis from Kik et al. only concluded that the moderate to good specificity but low sensitivity of CTA in comparison with DSA in diagnosing BCVI. Using CTA with higher channels (16–64) can not be more effective than lower channels (< 16).

The classification of BCVI in CTA or DSA was requested by Biffl et al. in 1999. It was applied for prognostication and comparison with repeated imaging (Table 2 and Figure 1) [8].

Biffl et al. injury grade	Definition
Grade I	Luminal irregularity or dissection with <25% luminal narrowing
Grade II	Dissection or intramural hematoma with ≥25% luminal narrowing
Grade III	Pseudoaneurysm
Grade IV	Occlusion
Grade V	Transaction with free extravasation

Table 2.

Denver grading scale for blunt cerebrovascular injury.

Figure 1.

Illustration of BCVI grading scale.

A retrospective cohort study from Ares et al. [16] with 312 patients includes that DSA is more accurate and sensitive than CTA in diagnosis BCVI. The DSA helps to avoid overtreatment in up to 41% of cases (CTA false positives), and can avoid missing injuries in up to 28% of cases (CTA false negatives). They introduced a protocol with DSA after the initial trauma and repeat within 2 weeks of injury to confirm the management of BCVI patients.

Abu et al. [17] listed several lesions that can mask or mimic focal vascular injuries on CTA. It resulted from artifact to preexisting pathologies and underlying normal anatomical variants.

Artifact: such as motion, swallowing, and pulsation during the performance. Dental implant artifacts should be removed before scanning the patient.

Preexisting nontraumatic pathology: Atherosclerotic plaque that makes the vessels narrow can mimic the appearance of a vascular injury. Atherosclerotic plaque can be distinguished from intramural hematoma. We can differentiate the two lesions by MRI. Underlying vasculitis or vascular dysplasia also makes a false diagnosis.

Underlying normal anatomical variants: Segments of vessel tortuosity, redundancy, and coiling can make a mistake as a small pseudoaneurysms. Preexisting vascular duplication and fenestration sometimes can result an emulating a double-lumen sign.

6. Treatment

To date, guidelines from the Western Trauma Associations [7] and EAST [10] recommend antithrombotic therapy, endovascular therapy, or surgical treatment based on the location and grade of injuries.

Recommendation from Brommeland et al. (2018) [8] suggests that a low-molecular weight heparin in antithrombotic doses within 24-48 h of the diagnosis followed by oral aspirin 75 mg daily. They also made a strong recommendation for the timing of antithrombotic therapy. Early usage as soon as possible is recommended even in the setting of severe traumatic brain injury or other solid organ injury.

In 2011, the ASA/ACCF/AHA/AANN/AANS/ACR/ASNR/CNS/SAIP/SCAI/SIR/SNIS/SVM/SVS guideline found level B for the treatment of stroke or transient ischemic attack patients with any anticoagulant agents (low-molecular-weight heparin, heparin, or warfarin) or an antiplatelet one (aspirin with or without extended-release dipyridamole, or clopidogrel exclusively) [18]. The duration of treatment lasted from 3 to 6 months after the trauma.

The practice management guideline from the Eastern Association for the Surgery of Trauma (2020) [12] suggested the benefit from the usage of antithrombotic versus no antithrombotic can decrease the risk of stroke (OR = 0.20–95%CI, 0.06–0.65 – p < 0.0001) and mortality (OR = 0.17–95%CI, 0.08–0.34 – p < 0.0001). And the guideline can not show any significant difference in the risk of stroke among patients with grade II or III injuries who underwent stenting as an adjunct to antithrombotic versus antithrombotic alone (OR = 1.63–95%CI, 0.2–12.14 – p = 0.63).

But the Western Trauma Association can not indicate any antithrombotic drugs for initial management. Aspirin may be available, but dual antiplatelet therapy (aspirin combined with clopidogrel) can be a safety and efficacy in a number of clinical situations [7].

Catapano et al. [19] indicated aspirin as the first-line therapy for patients with BCVI, if there were no contraindications, such as gastrointestinal bleeding, large ICH, or progression of ICH. After the treatment with aspirin, only 1/56 patients got stroke, 2/56 patients had progression of an intracerebral hemorrhage (neither required decompression) and 2/56 patients suffered from severe gastrointestinal bleeding. The result of follow-up of this aspirin group by vascular imaging showed the stable or improved levels of BCVI in 94% of patients. There were no delayed strokes or death. These authors concluded the aspirin-based management strategy for BCVI was efficacious and relatively safe.

Esnault et al. [2] made a decision to anticoagulation therapy on day 1.5, and 41% patients were indicated on arrival in the ICU. These authors believed that the latent period between injury and ischemia was observed mostly with 10–72 hours, the effect of this therapy can be easily monitored by partial thromboplastin time or anti-factors Xa activity, and in the setting of hemorrhagic complication or emergency surgery, this therapy can be quickly counteracted by protamine sulfate.

The choice of antiplatelet therapy or anticoagulation depends on the grade of BCVI, concomitant injuries, neurological symptoms, and the volume of infarcted territory at risk for hemorrhagic transformation (Table 3).

Injury grade	I	II	III	IV	V
Dever grading system	Irregularity of vessel wall dissection or IMH with <25% narrowing	Intraluminal thrombus, dissection, small AVF, or IMH with >25% narrowing	Pseudoaneurysm	Occlusion	Transection
CTA findings	Nonstenotic luminal irregularity, intimal flap, or wall thickening with <25% stenosis	Luminal hypodensity, intimal flap, or wall thickening with >25% stenosis	Eccentric contrast-filled outpouching limited by periarterial tissue	Lack of any intraluminal enhancement, carotid occlusions (abrupt or tapered), vertebral occlusion (usually abrupt)	Irregular extravascular collection of contrast, not limited by periarterial tissues, increases in density on delayed images if obtained
Stroke incidence (%)	8% cartotid; 6% vertebral	14% carotid; 38% vertebral	26% carotid; 27% vertebral	50% carotid; 28% vertebral	100% carotid; 100% vertebral
Initial therapy	Antithrombotic	Antithrombotic	Antithrombotic	Antithrombotic	Direct pressure on actively bleeding area until surgical intervention
Surgical/endovascular therapy	Not needed	Rare needed, but consider if neurologic symptoms, progression of dissection, or if refractory to therapy	Consider if symptomatic or if >1 cm	Stenting typically not beneficial, but thrombectomy ± stenting may be considered if stroke recognized within 6 h	Emergent intervention
Timing of follow-up imaging	7–10 days, then every 3–6 months until heal	7–10 days, then every 3–6 months until heal or definitive management	7–10 days, then every 3–6 months or based on symptoms	Based on symptoms	Based on symptoms
Long-term therapy	Antiplatelet therapy until healed	Antiplatelet therapy until healed or definitive surgical treatment	Antiplatelet therapy until healed or definitive surgical treatment	Lifelong antiplatelet	No data available, consider if symptomatic

Table 3.

Summarize the management of BCVI based on CTA findings.

AVF: arteriovenous fistula – IMH: intramural hematoma.

A study in 435 patients was treated with anticoagulation and 290 patients were treated with antiplatelet agents, Hanna et al. [20] resulted the hospital readmission rate (5.72 vs. 1.8%; p = 0.03), 6 months mortality rate (4.9 vs. 1.3%; p = 0.03) was significantly higher than in patients treated with antiplatelet agents when compared with those treated with anticoagulants. The similar result was manifested in the Cervical Artery Dissection in Stroke Study (CADISS) trial, however the difference did not mark a statistical significance [21].

The benefits of endovascular for patients with BCVI remain controversial because of its complication, stent predominance, and the rate of stroke. The indication of endovascular therapy includes: patients with a contraindication to antithrombotic agents, lesions that worsen or become symptomatic despite antithrombotic therapy, and lesions not amenable to surgical therapy. The grade II and III injuries should be treated by endovascular to decrease the risk of embolism and rupture by developing flow into the pseudoaneurysm. Endovascular can be performed for the grade V patients that are not surgically accessible. Patients with vessel occlusion also is the candidate of endovascular therapy to keep away from recanalization and embolic.

A conclusion from a study of Burlew et al. [22] showed that the stroke rate in the stent group (8.7%) and no-stent group (0.06%) was significantly different (p = 0.04). The authors suggest that intravascular stents should be reserved for the rare patient with symptomatology or a markedly enlarging pseudoaneurysm.

Surgical therapy has a limitation in the treatment of BCVI. No data, to date, can confirm the advantages of surgical performance. Carotid ligation, revascularization with direct, patch repair or bypass of the injured segment was recommended. In particular, the perioperative risk of hemorrhage may make surgical the preferred over endovascular stent, which requires antiplatelet treatment. We introduce some algorithms in management of BCVI (Figures 2 and 3).

Figure 2.

A flow-diagram summarizing for management of BCVI [8].

Figure 3.

The Denver health medical Center BCVI screening guideline [9].

7. Conclusion

BCVI is preventable cerebrovascular disorder by the application of screening recommendations, imaging modalities, and choosing a suitable repair therapy. CTA or DSA can be helpful to detect the morphology and location of the injuries. Early treatment of antithrombotic has been suggested to be both effective and safe, particularly in patient with minor and moderate injuries. The role of endovascular and surgical therapy remains controversial due to the lack of data.