Ischemic stroke caused by spontaneous anterior circulation intracranial arterial dissections: patient series

Abstract

BACKGROUND

Intracranial arterial dissections (IADs) are classically associated with the vertebrobasilar system, yet are a devastating cause of ischemic stroke within the anterior circulation. Current literature regarding the surgical management of anterior circulation IAD is lacking. As a result, data on 9 patients presenting with ischemic stroke due to spontaneous anterior circulation IAD between 2019 and 2021 were collected in a retrospective manner. Symptoms, diagnostic modalities, treatment, and outcomes are presented for each case. Patients who underwent endovascular procedures had 10-minute follow-up angiography performed to identify signs of reocclusion, which prompted initiation of glycoprotein IIb/IIIa therapy and stent placement.

OBSERVATIONS

Seven patients underwent emergent endovascular intervention (stenting: n = 5; thrombectomy alone: n = 2). The remaining 2 were managed medically. Two patients developed progressive flow limiting stenosis requiring further intervention, 2 developed asymptomatic progressive stenosis/occlusion with robust collateral formation and the remainder have patent vasculature upon follow up imaging at 6 to 12 months. Seven patients had a modified Rankin Scale score of 1 or less at the 3-month follow-up.

LESSONS

IAD is a devastating yet rare cause of anterior circulation ischemic stroke. The treatment algorithm proposed resulted in positive clinical and angiographic outcomes warranting future consideration and study in the emergent management of spontaneous anterior circulation IAD.

Arterial dissections are a well-known clinical entity resulting from a tear in the intimal wall and travel of blood between the tunica intima and tunica media creating an intramural hematoma.¹ Spontaneous intracranial arterial dissections (IADs), however, are a less known and less understood phenomena typically associated with the vertebrobasilar system, as the V4 segment accounts for approximately 50% of reported cases.^2,3 Anterior circulation IADs are far less represented in current literature.

IADs often occur in a young cohort of patients and can manifest as both ischemic stroke and subarachnoid hemorrhage (SAH).⁴ Ischemia is thought to arise from emboli, flow limiting stenosis, occlusion of the parent vessel by intramural hematoma or thrombus formation, or occlusion of small perforating vessels at the site of dissection. SAH results from rupture of pseudoaneurysms, which occur when the intramural hematoma extends into the adventitia.²

Reports of spontaneous IADs causing ischemic stroke in the anterior circulation are heterogenous and sparsely found within current literature.^3,5 As a result, management protocols are not well established.^6,7 To date, diagnosis is largely driven by findings seen on advanced imaging techniques, including digital subtraction angiography (DSA), computed tomography angiography (CTA), and magnetic resonance imaging high-resolution vessel wall imaging (MRI HR-VWI), an advanced MRI technique to assess for intramural hematoma.⁵

The purpose of this article is to provide a case series of spontaneous anterior circulation IADs including presenting signs/symptoms, diagnostic techniques, treatment approach and outcomes to enhance the current literature and a formal treatment algorithm for the endovascular management of IAD, particularly during an emergent interventional setting. To the best of our knowledge, the treatment algorithm to follow is novel, and the current series is the largest to focus solely on spontaneous IADs causing ischemia within the anterior circulation.

Study Description

Individual case summaries can be found in Table 1 and an additional summary of the case series as a whole can be found in Table 2.

TABLE 1.

Clinical case summaries of anterior circulation intracranial arterial dissections

Case No.	Presenting Exam	Location of IAD	Imaging Modalities	IV Thrombolysis	Treatment	TICI Score	FU Imaging	Clinical Outcome (mRS Score at 3 mos)	Radiographic Outcome at 3 Mos
1	NIHSS 8, rt hemiparesis, rt facial droop, dysarthria	Lt M1, additionally lt cervical to supraclinoid ICA	CTA, DSA	No	Intracranial thrombectomy w/ lt cervical ICA stent placement, antiplatelet therapy	3	DSA at 1 mon	Residual mild rt facial droop, presented 1 mo later w/ increased rt facial droop & right hemiparesis (5)	Progressive M1 flow limiting stenosis resulting in new symptomatic infarction requiring angioplasty & stenting
2	NIHSS 6, rt facial droop, rt arm drift, dysarthria	Lt M1	CTA, DSA	No	Thrombectomy w/ M1 stenting, antiplatelet therapy, complicated by intraop stent thrombosis	2a	DSA at 3 mos	Mild rt facial droop & 4+/5 rt hand grip (1)	Widely patent stent
3	NIHSS 10, rt MCA syndrome sparing lt-sided motor function	Rt M1	CTA, DSA, HR-VWI	No	Thrombectomy, antiplatelet therapy	3	DSA at 3 mos	Neurologically intact (0)	Widely patent M1
4	NIHSS 3, lt arm mild weakness & numbness	Rt M1	CTA, DSA, HR-VWI	No	Antiplatelet therapy	N/A	DSA at 3 mos	Mild lt arm numbness & 4+/5 grip (1)	Occluded M1 w/ formation of robust collateral flow
5	NIHSS 25, lt MCA syndrome	Lt M1	CTA, DSA, HR-VWI	Yes	Thrombectomy, antiplatelet therapy	3	DSA at 3 & 9 mos	Neurologically intact (0)	Progressive M1 stenosis to near occlusion w/ formation of collateral flow
6	NIHSS 11, lt MCA syndrome	Lt supraclinoid ICA	CTA, DSA, HR-VWI	No	Supraclinoid ICA stenting, antiplatelet therapy	3	DSA at 6 mos	Neurologically intact (0)	Widely patent stent
7	NIHSS 0, transient rt hemibody numb	Lt M1	CTA, DSA, HR-VWI	No	Antiplatelet therapy	NA	CTA on discharge	Neurologically intact, lost in FU (0 at discharge)	Stable M1 occlusion w/ collateral flow on discharge, lost in FU
8	NIHSS 17, lt MCA syndrome	Lt supraclinoid ICA	CTA, DSA	No	Supraclinoid ICA stenting, antiplatelet therapy	3	DSA at 6 mos	Neurologically intact (0)	Widely patent stent
9	NIHSS 9, lt MCA syndrome	Lt M1	CTA, DSA	Yes	Thrombectomy w/ M1 stenting, antiplatelet therapy	3	DSA at 3 mos	Residual mixed aphasia, disorientation, & rt arm weakness (3)	Progressive M1 flow limiting stenosis w/poor collateral formation requiring STA-MCA bypass

FU = follow-up; NA = not applicable.

TABLE 2.

Case series summary

Variable	Value
Average age in yrs	43.5 ± 21.9
Average NIHSS score	9.9 ± 7.5
IV thrombolysis administration: yes/no	2/7
TICI score
3	6
2b	0
2a	1
1	0
0	0
NA	2
Thrombectomy performed: yes/no	5/4
Stent placement at index presentation: yes/no	4/5
mRS at 3 mos
0	5
1	2
2	0
3	1
4	0
5	1
Good angiographic outcome at 3 mos of intracranial stents placed at index presentation: yes/no*	3/1

^*Angiographic outcomes were considered favorable if there was no angiographic evidence of disease progression or in-stent stenosis at 3 months.

Patient Selection and Variables

A total of 9 cases of anterior circulation IADs causing ischemic stroke were collected in a retrospective manner. A total of 460 cases of acute ischemic stroke caused by large vessel occlusions (LVO) presented between the years 2019 and 2021. These cases were identified as patients presenting with new neurological deficits and CTA evidence of LVO. Medium and small vessel occlusions were excluded, as they were not candidates for thrombectomy. The appropriateness for endovascular interventions in the setting of LVO was determined by an attending neurosurgeon per stroke guidelines regarding last known well times, size of core infarct, etc. The decision to administer intravenous (IV) thrombolysis was made by an attending stroke neurologist per stroke guidelines, and discussions of which are outside the scope of this article. Standard to the care of acute ischemic stroke, all patients underwent comprehensive workup to identify etiology (i.e., atherosclerotic disease, hypercoagulability, cardioembolic, primary vascular malformation, etc.). Only those whose workup did not reveal an alternative etiology and who were devoid of trauma were included, as agreed upon by both an attending neurosurgeon and stroke neurologist. IADs within the posterior circulation were excluded, as they are more commonly recognized and outside the scope of this case series.³ Additionally, to be included, an attending neurosurgeon, stroke neurologist, and neuroradiologist had to agree that the diagnostic criteria of IAD described below was met.

Once included, each patient’s initial National Institutes of Health Stroke Scale (NIHSS) score was recorded in addition to their emergent endovascular management and subsequent thrombolysis in cerebral infarction (TICI) score if thrombectomy was performed, location of the IAD, medical management, other imaging modalities utilized for diagnosis, follow-up imaging used to assess for favorable radiographic outcome, and modified Rankin Scale (mRS) score at 3 months after the index event. A favorable mRS score was considered <2. A favorable radiographic outcome was considered stable or improved vessel caliber without flow limiting stenosis when compared to index imaging.

Patient Population

The average age of presentation was 43.5 ± 21.9 years (youngest: 15 years old, oldest: 84 years old). Two were female, whereas the other 7 were male. Five (56%) were White, 3 (33%) were Black, and 1 (11%) was Hispanic. Common comorbidities include smoking, hypertension, hyperlipidemia, and substance use. Average initial NIHSS score was 9.9 ± 7.5 (low: 0, high: 25). IAD affected the left M1 segment (n = 5), right M1 segment (n = 2) and left supraclinoid internal carotid artery (ICA; n = 2). All patients underwent CTA and DSA, whereas 7 underwent HR-VWI.

Diagnosis of IAD

The diagnosis of IAD was made only if 4 or more imaging findings were encountered (Table 3, Fig. 1).^{2,3,5,6,8–23} An addition to this list of diagnostic criteria is an intraoperative angiographic finding not previously described that was encountered when using endovascular interventional techniques described as follows: angiography through a catheter proximal to an LVO (i.e., intermediate or guide catheter) with a microcatheter tracked distally to the occlusion reveals a patent parent vessel (Fig. 1). This technique is similar to that portrayed by Labeyrie et al.¹⁶ and Bernard et al.,²² which includes angiography through a deployed stentriever across an area of LVO revealing a patent parent vessel. Both functions to elevate the dissection flap restoring patency to the vessel. One or both of these angiographic findings were present in all patients who underwent thrombectomy in the current case series.

TABLE 3.

Imaging characteristics suggestive of intracranial arterial dissection

Imaging Characteristic
1. Luminal irregularities causing fusiform/irregular dilation*
2. Luminal irregularities causing focal stenosis*
3. Luminal irregularities causing focal stenosis w/ associated areas of dilation (i.e., “string of pearls” sign)*
4. Long segment stenosis w/ luminal irregularities*
5. Visualized intimal flap (i.e., “double lumen” sign)
6. Occlusion w/ adjacent irregular dilation or stenosis
7. Rapid change in arterial morphology on FU imaging
8. Tapering occlusion or stenosis (i.e., “flame” sign)
9. T1 hyperintense eccentric wall thickening on MRI HR-VWI indicating presence of intramural hematoma
10. Normalization of arterial caliber after stenting
11. No clot return w/ embolectomy

^*Luminal irregularities are caused by intramural hematoma.

FIG. 1.

Findings on DSA revealing intracranial arterial dissection. A: Anteroposterior (AP) left ICA DSA reveals an intimal flap (arrows) within the M1 segment of the MCA in case 1. B: Lateral left ICA DSA revealing a tapered area of focal stenosis (arrow) within the supraclinoid segment in case 6. C: Lateral left ICA DSA demonstrating an intimal flap and intramural hematoma (arrows) creating areas of stenosis/dilation within the ICA and M1 segment of the MCA. An exemplary case not included in the current series due to no LVO at presentation. D: AP right ICA DSA showing fusiform dilation with proximal stenosis of the A1 segment of the anterior cerebral artery (arrows). An exemplary case not included in the current series due to no LVO at presentation. E: AP right ICA DSA showing an ICA terminus occlusion prior to deployment of a stentriever in case 3. F: AP right ICA DSA showing restoration of the ICA terminus/MCA patency after a deployed stentriever elevated the intimal flap that previously caused an ICA terminus occlusion in case 3.

Treatment

A summary of the formal treatment algorithm employed can be found in Fig. 2. Two of 9 patients presented with an NIHSS score <6. Consequently, the risks of endovascular intervention were believed to outweigh the benefits, thus each was managed conservatively with dual antiplatelet therapy (DAPT) alone.^3,7,20,24,25 Seven of 9 patients underwent emergent endovascular intervention. Thrombectomy with stent placement was performed in 2 of 7, thrombectomy alone was performed in 3 of 7, and stent placement alone was performed in 2 of 7. All patients who underwent stent placement demonstrated angiographic evidence of vessel reocclusion within 10 minutes of attempted thrombectomy. In preparation for stent placement, a glycoprotein (GP) IIb/IIIa inhibitor bolus was given immediately followed by initiation of a continuous infusion. The next morning, the infusion was transitioned to DAPT with a P2Y-12 inhibitor and aspirin consistent with previous reports.⁷ A general summary of this treatment algorithm is as follows: if a patient presenting with NIHSS score >6 and an LVO caused by anterior circulation IAD, standard thrombectomy techniques would be used emergently. Once vessel patency has been achieved, and if the aforementioned diagnostic criteria for IAD were met, then the follow-up angiography would be performed 10 minutes later. If the site of LVO and IAD remained patent, stenting would be deferred. If the vessel reoccluded, or became progressively more stenotic, then GP IIb/IIIa inhibitor therapy would be initiated followed by stent placement in the acute setting. Patients with stents would be transitioned to DAPT the following day.

FIG. 2.

A formal treatment algorithm for ischemic stroke cause by anterior circulation IAD. *Indications: last known well <6 hours ago, Alberta Stroke Program Early CT Score (ASPECTS) ≥6, last known well >6 hours ago and <24 hours ago with mismatch ratio >1.8 on perfusion imaging, NIHSS ≥6 at time of procedure. Systemic thrombolysis decision-making excluded, as decision to administer is independent of surgical decision-making.

Intraoperative stent thrombosis complicated case 2 resulting in initial TICI 2a recannulization. Upon routine follow-up angiography, all residual thrombus resolved with widely patent stent and intracranial vasculature. In all other cases in which thrombectomy or stenting was performed, TICI 3 recannulization was achieved. Of the 2 patients who underwent thrombectomy alone, one patient’s occluded vessel remained patent after a 10-minute period of intraoperative observation, thus stenting was deferred in favor of DAPT alone. The other initially showed angiographic signs of vessel reocclusion, although the vessel lumen stabilized once GP IIb/IIIa inhibitor therapy was initiated, thus stenting was deferred. This patient was transitioned to DAPT the next morning.

Patients who did not undergo stent placement and remained neurologically stable without angiographic evidence of disease progression were transitioned from DAPT to aspirin monotherapy after 3 months, while those who underwent stent placement and demonstrated angiographic evidence of stent patency on follow-up imaging were transitioned to aspirin monotherapy after 6 months. If disease progression or in-stent stenosis occurred, DAPT was continued with plans to reevaluate on a case-by-case basis via clinical monitoring and repeat imaging.

Systemic thrombolysis is excluded from the discussed treatment decisions and this article, as the study of its efficacy in treating IAD remains ongoing and beyond the scope of endovascular management of IAD.²⁶

Outcomes

Aside from cases 1 and 7, all underwent routine follow-up DSA at either 3 or 6 months from initial presentation. Case 1 presented with an occlusive left M1 IAD and flow limiting left cervical ICA dissection requiring emergent thrombectomy and cervical ICA stent placement, respectively, then re-presented with worsening right facial droop and hemiparesis 1 month after discharge in the setting of strict DAPT compliance. DSA was performed, which revealed a widely patent carotid stent, however, progressive flow limiting left M1 stenosis was noted, which required angioplasty and stenting. Case 7 was lost to follow-up, whereas the rest continue to be followed on an outpatient basis. No hemorrhagic complications were encountered.

Functional outcomes were considered favorable if mRS score at 3 months was <2. All initially had improved neurological status from their index presentation. Five of 9 patients have made a full recovery with no detectable neurological deficits, a mRS score of 0. Patient 9 has a mRS score of 3 at 3-month follow-up, and patient 1 has an mRS score of 5. The remaining patients have maintained their independence despite mild residual symptoms (mRS score of 1).

Angiographic outcomes were considered favorable if there was no angiographic evidence of disease progression or in-stent stenosis at 3 months. Case 7 was managed with DAPT alone, was neurologically intact on the day of discharge, and repeat CTA performed prior to discharge revealed a stable left M1 occlusion with extensive collateralization. Three of 4 patients who underwent intracranial stenting at their index presentation continue to show angiographic evidence of a widely patent stent with robust anterograde flow. Case 9, however, underwent emergent M1 stenting and showed progressive flow limiting in-stent stenosis with poor collateralization on follow-up DSA requiring superficial temporal artery-middle cerebral artery (STA-MCA) bypass grafting. Of the 5 who did not undergo intracranial stenting at their index presentation, follow-up imaging revealed widely patent vasculature in 1 of 5, whereas 3 of 5 were found to have asymptomatic progressive stenosis or occlusion with robust collateral formation. The remaining 1 of 5 (case 1) presented with new ischemic symptoms 1 month after discharge from the index procedure and required intracranial stenting at that time, as described above.

Discussion

Observations

Spontaneous anterior circulation IAD remains an uncommon, yet devastating cause of ischemic stroke. The current series provides a detailed collection of cases to draw attention to the possibility of IAD as an etiology of ischemic stroke and provide a formal guide to their emergent management, a feat lacking in literature. To the best of our knowledge, this is the first and largest report with a sole focus on anterior circulation IAD.

IAD must be promptly recognized as a potential etiology for ischemic stroke and immediately considered in younger patients.² The initial emergent management includes standard stroke workup in the form of noncontrast CT and CTA. CTA may reveal more classic features of dissection, including tapering occlusions or a “flame sign,” a dissection flap, mural hematoma, etc.²² However, CTA may also simply demonstrate an LVO. LVOs often result in significant ischemia and clinical deficits that warrant emergent angiography and likely intervention. This allows the interventionalist the ability to use standard endovascular techniques to aid in the diagnosis of IAD when clinical suspicion is high. For example, normalization of arterial caliber after stentriever deployment and no clot return during thrombectomy, as described by Bernard et al.²² in the 2012 Childhood Arterial Ischemic Stroke Standardized Classification and Diagnostic Evaluation (CASCADE) guidelines. In addition to this phenomenon, we propose that a patent parent vessel seen on angiography with a microcatheter tracked distally to a LVO should be added to this list of diagnostic criteria. Functionally, this provides the same mechanism as a deployed stentriever, as both elevate the intimal flap restoring anterograde flow. Conversely, when using these endovascular techniques, the deployed stentriever may appear deformed and stenotic representing an underlying atherosclerotic steno-occlusion. The acute endovascular management of underlying atherosclerotic disease does not include stenting, thus it is critical to recognize these different pathologies.²⁷

Once IAD has been recognized intraoperatively, the interventionalist should continue to employ thrombectomy techniques as needed to restore patency and anterograde flow within the parent vessel of an LVO. Once achieved, however, we recommend intraoperative monitoring via follow up angiography 10 minutes after thrombectomy was performed, as it allows the interventionalist to identify the patient who will go on to reocclude their symptomatic vessel and recognize when stenting may be indicated.

Good functional and radiographical outcomes after stenting IADs has been reported. Despite promising outcomes, reports in current literature remain small in sample size, nonspecific regarding IAD anatomical location and indications for stent placement vary.^4,7,16,28 For example, Jeon et al.⁴ presents a series of good functional outcomes with stenting of both extracranial and intracranial arterial dissections, however, their data regarding spontaneous IAD of the anterior circulation are limited to just 1 patient. Furthermore, Labeyrie et al.¹⁶ presented a series of 7 patients with IAD who underwent stenting, Forbrig et al.²⁸ presented a series of both anterior and posterior circulation IAD who underwent stenting as a rescue maneuver, Kim et al.¹² presented a series of 7 anterior circulation IADs who underwent stenting and, most recently, Bernava et al.⁷ reported a series of 6 patients with anterior circulation IAD who underwent stenting. All report good functional and radiographical outcomes, however, they lack rigid criteria for stent placement. Due to these small sample sizes and informal treatment protocols, standard of care remains unclear.⁷

Stent placement during an emergent intervention is a challenging intraoperative scenario to manage. In the current series, 4 of 7 patients who underwent endovascular intervention required intracranial stenting after 10-minute follow-up angiography revealed evidence of reocclusion. In this scenario, a GP IIb/IIIa inhibitor bolus was given followed initiation of a continuous infusion in preparation of stenting. All patients who underwent GP IIb/IIIa inhibitor therapy were transitioned to DAPT the next day. With the exception of 1, all patients exhibited significant neurological recovery with patent vasculature upon 3- to 6-month follow-up DSA consistent with previous reports,^4,7,16,28 and no patient suffered from hemorrhagic consequences. Conversely, when the vessel caliber remained stable after 10-minute follow-up angiography or stabilized after initiation of antiplatelet therapy, stenting was deferred in favor of antiplatelet therapy alone.

Medical management is the first line treatment of IADs in both pediatric and adult patients.¹¹ Medical management of IAD consists of antiplatelet therapy, as per American Stroke Association guidelines.²⁵ Additionally, patients who undergo stenting in the United States are typically treated with DAPT for at least 6 months followed by aspirin monotherapy for life.²⁹ In this setting, SAH from pseudoaneurysm rupture after stenting is a severe complication to consider, as the pseudoaneurysm is unstable with significant risk of rerupture (approximately 70%) and mortality (approximately 63%), although antiplatelet agents must be continued given the significant risk of in-stent thrombosis and ischemic events.^5,30 Without stent placement, however, the benefits of minimizing the risk of rebleeding by holding DAPT now outweigh the risk of ischemic injury. As such, despite favorable outcomes with stent placement, it is in the patient’s best interest to avoid stent placement and mandatory antiplatelet therapy whenever possible.

IAD of the anterior circulation continues to be a challenging pathology to face, as it has historically been under recognized as an etiology for stroke, and there remains no uniform diagnostic or treatment guidelines. Medical management alone remains the mainstay of IAD treatment, as it may be more safely held in the event of hemorrhage without the presence of a stent.^11,25 Additionally, even when disease progression occurs (i.e., progressive stenosis), DAPT has demonstrated an ability to slow progression enough to allow compensatory collateralization to form avoiding neurological injury in this case series.

Lessons

The current case series highlights the importance of considering IAD as a cause of anterior circulation ischemic stroke and provides a formalized algorithm to guide emergent management of this rare pathology. The proposed diagnostic steps and treatment algorithm resulted in overall favorable clinical and angiographic outcomes, with the majority of patients demonstrating a mRS score <2 and no angiographic evidence of disease progression at follow-up. Given the small sample size, however, further study is warranted.

Limitations to the current case series should be considered when interpreting the outcomes and treatment algorithm presented. First, patient selection occurred in a retrospective manner within a single institution. Additionally, the rarity of ischemic stroke from spontaneous anterior circulation IADs led to a small sample size.

Acknowledgments

The authors would like to acknowledge the support staff including the anesthesiologists, neurologists, emergency medicine physicians, nurses, and interventional radiology technicians whose contributions make the emergent management of patients suffering from stroke safe and efficient.

Disclosures

Dr. Bender reported personal fees from Stryker Neurovascular outside the submitted work.

Author Disclosures

Conception and design: Furst, Bender, Mattingly. Acquisition of data: all authors. Analysis and interpretation of data: Furst, Bender. Drafting the article: Furst, Ellens. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Furst. Administrative/technical/material support: Mattingly. Study supervision: Mattingly.