Abstract
Background
Emergency stent placement in the extracranial internal carotid artery in combination with anterior circulation thrombectomy is a routine procedure. Yet, precise indications and clinical safety in this setting remains controversial. Present data for mechanical thrombectomy include few studies with acute stenting of tandem occlusions. We evaluated the feasibility, safety and clinical outcome of this endovascular treatment in a retrospective analysis of all consecutive cases at a comprehensive stroke centre.
Methods
This was a retrospective analysis of all consecutive patients with acute extracranial carotid artery occlusion including acute dissection or high-grade stenosis and concomitant intracranial large-vessel occlusion treated with emergency carotid stenting and intracranial mechanical thrombectomy between November 2007 and May 2015.
Results
A total of 63 patients with a median age of 67 years (range 33–84 years) were treated. Of these, 33 (52%) patients had concomitant intravenous thrombolysis with recombinant tissue-type plasminogen activator initially. Median admission National Institutes of Health Stroke Scale was 14 (range 1–29). Median time from stroke onset to recanalization was 408 minutes (range 165–1846 minutes). Procedure time was significantly shorter after intravenous thrombolysis (110 minutes [range 15–202 minutes] vs. 130 minutes [range 60–280 minutes]; p = 0.02). Three (5%) patients experienced post-procedural symptomatic intracerebral haemorrhage. In 55/63 (87%) patients, a score of ≥2b on the Thrombolysis in Cerebral Infarction scale could be achieved. Eight (13%) patients died, five (8%) during the acute phase. A total of 29/63 (46%) patients showed a favourable outcome (modified Rankin Scale score of 0–2) after three months.
Conclusions
Our single-centre retrospective analysis of emergency stent placement in the extracranial internal carotid artery in combination with anterior circulation thrombectomy demonstrated high technical success, reasonable clinical outcomes and acceptable rates of symptomatic intracranial haemorrhage in carefully chosen patients which are triaged interdisciplinary based on clinical and computed tomography imaging criteria. This warrants further study in a randomised prospective trial.
Keywords: Tandem occlusion, acute extracranial carotid artery occlusion, emergency carotid stenting, intracranial mechanical thrombectomy, ischemic stroke
Introduction
Acute ischemic stroke due to tandem occlusion, defined as occlusion or high-grade stenosis (70–99%; North American Symptomatic Carotid Endarterectomy Trial criteria) of the internal carotid artery (ICA) with concurrent embolic occlusion of a major intracranial vessel represents 10–20% of stroke patients.1,2 Intravenous thrombolysis (IVT) alone rarely yields successful recanalization.3,4 Timely and effective reperfusion is necessary to reverse the ischemic penumbra and to increase the chance of a favourable clinical outcome.5 Endovascular treatment has been proven to have high recanalization rates and better clinical outcomes in patients with large vessel occlusions when compared with medical therapy alone in many consecutive randomised controlled trials.6–10 Endovascular therapy in acute tandem occlusions necessitating acute ICA stenting comprises two different concepts: to stent first and then conduct mechanical thrombectomy (MT; ‘antegrade approach’) or vice versa (‘retrograde approach’).11–23 Besides the complexity of the procedure, a major concern is the immediate need for antiplatelet therapy to avoid in-stent thrombosis in the setting of an acute ischemic stroke.
The aim of this study was to assess the feasibility, safety and clinical outcome of emergency stenting of the cervical ICA in combination with anterior circulation thrombectomy.
Methods
Patient selection
In a retrospective cross sectional analysis (intention-to-treat basis), we evaluated all consecutive stroke patients who underwent emergency stenting of the extracranial ICA in combination with anterior circulation thrombectomy between November 2007 and May 2016 at our institution.
Patients were either admitted directly (12/63; 19%) or transferred from one of six referring hospitals within the region or occasionally from outside the primary catchment area (51/63; 81%).
All patients arriving from the referring hospitals had a non-enhanced computed tomography (NECT) scan performed before being transferred to our department. In the later part of the series, patients also had a computed tomography angiography (CTA) before transfer. Patients with signs of intracerebral haemorrhage (ICH) or major infarction were not referred. Patients who were not eligible for IVT but otherwise treatable were transferred if an endovascular treatment could be expected to be initiated within eight hours after symptom onset. Five patients were treated beyond this window due to secondary worsening within 24 hours of the initial onset. Patients with a National Institutes of Health Stroke Scale (NIHSS) score of 8–30 (from 2010, changed to 6–25) without severe co-morbidities were considered for MT. An exception was made for selected patients with a NIHSS score of <6 if the symptoms included aphasia.
All patients arriving from outside hospitals bypassed the emergency room (ER) and were transferred directly to the department of neuroradiology, where a stroke neurologist and anaesthesiology met up. A neurological examination was followed by NECT complemented with CT perfusion (CTP) and CTA. If a CTA had been realised already at the referring hospital, it was repeated only if the patient had improved clinically.
Patients admitted directly (i.e. primarily not as stroke alert patients) were examined clinically in the ER, and then immediately transferred to the department of neuroradiology for the same imaging stroke protocol. If a patient was eligible for IVT with recombinant tissue-type plasminogen activator (rtPA), it was initiated immediately after the scanning.
The decision of whether to proceed with MT was made jointly by the stroke neurologist and the neurointerventionist. MT was considered for all patients with remaining symptoms, a large-vessel occlusion and salvageable brain parenchyma (penumbra) as interpreted from the CT, CTA and CTP images (CTP mismatch concept). Major infarction, defined as >1/3 of MCA territory on NECT, used to be an exclusion criterion in the beginning of this series. As experience grew and robust data about MT and its safety became available in the literature and from our own institutional database in the years 2010–2012, the 1/3 MCA rule was eclipsed in favour of the CTP mismatch concept. The Alberta Stroke Program Early CT Score (ASPECTS) was not used as a criterion for or against endovascular treatment. Ongoing IVT was terminated when a guide catheter had been positioned and it was likely that the MT would be technically feasible.
The study was approved by the institutional research ethics committee.
Endovascular treatment regimen and procedural data
Endovascular treatment was routinely performed in conscious sedation and in a few cases under general anaesthesia. A dedicated team of neuro-anaesthesiologists was available for all neurointerventions. Conscious sedation was preferred when the patient was compliant. General anaesthesia was used in agitated patients and those who could not follow instructions during the procedure. Assessment of the target vessel was obtained by digital subtraction angiography and compared with the prior CTA with respect to clot location and characteristics of the occlusions. The extracranial carotid lesion was classified as arterial dissection or atherosclerotic lesion. For most cases, the standard MT procedure began by placing the tip of an 80-cm long introducer sheath, mostly an Arrow 8F (Arrow International, Reading, PA) in the common carotid artery (CCA), just below the bifurcation, in which an 8F or 9F Merci balloon guide catheter (Concentric Medical/Stryker Neurovascular, Kalamazoo, MI) was inserted with its tip positioned in the proximal ICA. The carotid lesion was passed with a Terumo .035 guidewire, and then the Merci catheter was pushed through the stenosis and was thus occlusive. When the stenosis was very calcified, pre-dilatation was sometimes necessary. The self-expandable carotid stent (Precise; Cordis Corporation, Miami Lakes, FL; in a few cases, Wallstent or Adapt-Stent; Boston Scientific, Natick, MA) was usually placed after the thrombectomy, while retracting the Merci catheter. In patients requiring an antegrade approach (stent first), the balloon of the Merci guider was inflated in the CCA before stent placement. All patients received ICA stent placement. Stents were balloon dilated when needed to ensure adequate width, wall apposition and flow. Thrombectomy was performed using stent retrievers in 55/59 (93%) procedures and repeated as needed (Solitaire FR and MindFrame Capture, Medtronic/ev3, Irvine, CA; Trevo variants, Stryker, Kalamazoo, MI; EmboTrap, Neuravi, Galway, Ireland). In 4/59 (7%) cases, MT was performed using the Merci Retrievers (Concentric Medical/Stryker Neurovascular, Mountain View, CA). In 4/63 (6%) cases, no MT was conducted because of spontaneous dissolution of the thrombus after carotid stent placement. Carotid stenting was performed before 17/63 (27%) or after 46/63 (73%) intracranial MT at the operator’s discretion. Femoral hemostasis was ensured with vascular closure systems or manual compression. The total number of thrombectomy passes and quality of reperfusion was recorded. Successful recanalization was defined as a score of 2b-3 on the Thrombolysis in Cerebral Infarction (TICI) scale.24
Antiplatelet medication
During the intervention, the patient received half of the recommended bolus dose (0.125 mg/kg body weight) of abciximab but no infusion, followed by acetylsalicylic acid (ASA) directly after the procedure (bolus of 300 mg and then 75 mg daily for a minimum of six months) and clopidogrel (bolus of 300 mg and then 75 mg daily for a minimum of three months) after 12–24 hours when a routine follow-up NECT scan did not reveal a significant hematoma.
Follow-up imaging
All patients obtained CT and/or magnetic resonance imaging at 18 ± 6 hours after the intervention. Control scans were screened for ICH and classified as ‘symptomatic’ according to European Cooperative Acute Stroke Study criteria (any apparently extravascular blood in the brain or within the cranium that was associated with clinical deterioration, as defined by an increase of ≥4 points on the NIHSS score, or that led to death and that was identified as the predominant cause of the neurologic deterioration).25
Clinical outcome
A stroke neurologist examined all patients clinically on admission and discharge (NIHSS and modified Rankin Scale [mRS]) from the stroke centre and the rehabilitation unit (follow-up mRS at 90 days). Discharge NIHSS was available in 51/63 (81%), discharge mRS in 62/63 (98%) and mRS at 90 days in 61/63 (97%) patients. Good clinical outcome after three months was defined as a mRS score of 0–2.
Statistical analysis
The determination of the number of cases was based on the availability of patient cases. Statistical significance was set at p < 0.05. The significance of differences between the patient groups was determined with the two-tailed Fisher’s exact test, Student’s t-test or Wilcoxon test where appropriate. The statistics were performed with the use of MedCalc Software v15.8 (MedCalc, Ostend, Belgium).
Results
Study population
Sixty-three patients were treated between November 2007 and May 2015, comprising six (10%) wake-up strokes where the ‘last well time’ was taken for time interval calculations, and another four (6%) patients with unknown symptom onset which were excluded from the respective calculations. The median age of the patients was 67 years (range 33–84 years); 49/63 (78%) were male. Patients presented after a median of 212 minutes (range 0–1203 minutes) with a median NIHSS score of 14 (range 1–29). Distal occlusion sites were: MCA M1 in 35/63 (56%), MCA M2 in 9/63 (14%) and Carotid-T in 19/63 (30%). Proximal ICA dissections were identified in 9/63 (14%) cases. Concomitant IVT was applied in 33/63 (52%) strokes. The median time groin puncture to recanalization time was 118 min (range: 15-280 min); overall, the median symptom onset to recanalization was 408 minutes (range 165–1846 minutes). Median procedural timings were significantly shorter in patients with concomitant IVT (110 minutes; range 15–202 minutes) in comparison with patients who were ineligible for IVT (130 minutes; range 60–280 min; p = 0.02). This finding did not translate into a statistically significant improvement of the rate of good clinical outcome (55% vs. 40%; p = 0.3). A successful angiographic recanalization was achieved in 55/63 (87%) cases, comprising 18/63 (29%) patients with TICI 3. Carotid stenting was performed before MT in 17/63 (27%) and after MT in 46/63 (73%) at the interventionist’s discretion. The course of action did not lead to different procedural timings (antegrade approach 110 minutes [range 15–208 minutes] vs. retrograde approach 125 minutes [range 45–212 minutes]); p = 0.42) but to a tendency in the rate of good clinical outcome after 90 days in favour of the retrograde approach (52% vs. 29%, p = 0.16; Table 2). Furthermore, in 4/17 (24%) patients treated in antegrade fashion, a spontaneous thrombus dissolution was observed. Median NIHSS was 8 (range 0–22) and mRS 4 (range 2–6) on discharge. Results are summarised in Tables 1 and 2.
Table 2.
Procedural data and clinical outcome.
| Timings | |
| Symptom onset to admission (minutes), median (range) | 212 (0–1203) |
| Groin puncture to final recanalization (minutes), median (range) | 118 (15–280) |
| Subgroup with IVT: | |
| Groin puncture to final recanalization (minutes), median (range) | 110 (15–202) |
| Subgroup without IVT: | |
| Groin puncture to final recanalization (minutes), median (range) | 130 (60–280) |
| Symptom onset to final recanalization (minutes), median (range) | 408 (165–1846) |
| Angiographic results | |
| Stent retriever thrombectomy, n/N (%) | 55/59 (93) |
| Merci Retriever thrombectomy, n/N (%) | 4/59 (7) |
| Spontaneous thrombus dissolution, n/N (%) | 4/17 (24) |
| Carotid stenting antegrade approach, n/N (%) | 17/63 (27) |
| Carotid stenting retrograde approach, n/N (%) | 46/63 (73) |
| Number of thrombectomy passes, median (range) | 2 (1–10) |
| Final TICI 2b/3, n/N (%) | 55/63 (87) |
| Final TICI 3, n/N (%) | 18/63 (29) |
| Final TICI 2b/3, n/N (%) antegrade approach | 14/17 (82) |
| Final TICI 3, n/N (%) antegrade approach | 0/17 (0) |
| Final TICI 2b/3, n/N (%) retrograde approach | 41/46 (89) |
| Final TICI 3, n/N) (%) retrograde approach | 18/46 (39) |
| Adverse events | |
| ENT, n/N (%) | 3/63 (5) |
| sICH (ECASS criteria), n/N (%) | 3/63 (5) |
| Clinical outcome | |
| Discharge NIHSS, median (range) | 8 (0–22) |
| Discharge mRS, median (range) | 4 (2–6) |
| 90-day mRS, median (range) | 3 (0–6) |
| 90-day mRS 0–2, n/N (%) | 29/63 (46%) |
| 90-day mRS 0–2, n/N (%) antegrade approach | 5/17 (29%) |
| 90-day mRS 0–2, n/N (%) retrograde approach | 24/46 (52%) |
TICI: Thrombolysis in Cerebral Infarction scale; ENT: embolisation to new territory; sICH: symptomatic intracerebral haemorrhage.
Table 1.
Patient characteristics on admission.
| Age (years), median (range) | 67 (33–84) |
|---|---|
| Male sex, n/N (%) | 49/63 (78) |
| Arterial hypertension, n/N (%) | 31/63 (49) |
| Atrial fibrillation, n/N (%) | 4/63 (6) |
| Diabetes mellitus, n/N (%) | 11/63 (17) |
| Dissection of carotid artery, n/N (%) | 9/63 (14) |
| M1 occlusion, n/N (%) | 35/63 (56) |
| M2 occlusion, n/N (%) | 9/63 (14) |
| Carotid-T occlusion, n/N (%) | 19/63 (30) |
| IVT bridging, n/N (%) | 33/63 (52) |
| Initial NIHSS, median (range) | 14 (1–29) |
| mRS pre-stroke, median (range) | 0 (0–5) |
| Wake-up stroke and stroke of unknown onset, n/N (%) | 10/63 (16) |
IVT: intravenous thrombolysis; NIHSS: National Institutes of Health Stroke Scale; mRS, modified Rankin Scale.
Clinical outcome
A total of 29/63 (46%) patients had a good clinical outcome at 90 days. They were significantly younger (63 years [range 33–79 years] vs. 69 years [range 51–82 years]; p < 0.01) and featured a lower initial mean NIHSS of 12 (range 1–29) by trend compared with a score of 15 (range 8–26; p = 0.09). Patients with dissection showed a trend to good clinical outcome after 90 days (p = 0.08). Procedural timings, atrial fibrillation, hypertension and diabetes mellitus had no effect on clinical outcome. The number of stent retriever passages had no significant impact on clinical outcome (p = 0.49). In-hospital mortality accounted for 5/63 (8%); a total of 8/63 (13%) patients were dead after three months (Table 3).
Table 3.
Clinical outcome at 90 days and associated factors.
| mRS 0–2 (90 days) | mRS 3–6 (90 days) | p-Value | |
|---|---|---|---|
| Age (years), median (range) | 63 (33–79) | 69 (51–82) | 0.004 |
| Groin puncture to final recanalization (minutes), median (range) | 116 (45–215) | 120 (15–280) | 0.9 |
| Symptom onset to final recanalization (minutes), median (range) | 435 (165–1846) | 375 (200–1510) | 0.68 |
| Atrial fibrillation, n/N (%) | 4/29 (14) | 0/32 (0) | 0.04 |
| Arterial hypertension, n/N (%) | 15/29 (52) | 16/32 (50) | 1 |
| Diabetes mellitus, n/N (%) | 4/29 (14) | 7/32 (22) | 0.51 |
| Initial NIHSS, median (range) | 12 (1–29) | 15 (8–26) | 0.09 |
| IVT, n/N (%) | 17/29 (59) | 14/32 (44) | 0.31 |
| ICA dissection, n/N (%) | 7/29 (24) | 2/32 (6) | 0.08 |
| No. of thrombectomy passes, median (range) | 2 (0–7) | 2 (0–10) | 0.42 |
Adverse events
Embolisation to new territory was recorded in 3/63 (5%) cases. Periprocedural in stent thrombosis was ascertained in 4/63 (6%) procedures. The control CT scans revealed a small petechiae (HI1) in 1/63 (2%), a hemorrhage (coagulum) with mass effect, with (a) <30% of the infarcted area with mild space-occupying effect (PH1) in 4/63 (6%) and (b) >30% of the infarcted area with significant space-occupying effect (PH2) in 2/63 (3%) patients. Of these seven hemorrhages, only 3 (5%) were classified as symptomatic ICH (sICH); all sICH led to death in the acute phase. IVT had no effect on the rate of sICH (p = 0.6).
Discussion
Stroke patients with intracranial large-artery occlusion benefit from MT in addition to the individual optimum medical therapy.6–10 Between 10% and 20% of patients with an intracranial vessel occlusion also carry an additional occlusion or high-grade stenosis of the extracranial ICA, and these patients are prone to long-term dependency if vascular recanalization is not achieved.1 Tandem occlusions respond poorly to IVT alone, frequently resulting in a high rate of unfavourable clinical outcome.26,27 Acute ICA stent placement and pre stent retriever devices have been explored, yielding acceptable rates of technical success in the cervical ICA but overall limited clinical results due to relatively low rates of successful intracranial recanalization.28,29 Meanwhile, a substantial evolution of aspiration catheters and clot extraction devices has taken place, in particular the introduction of stent retrievers.17–19,30 Several stroke centres have reported their experience with tandem occlusion treatment with different techniques.11–21 Reperfusion in these series was successful in up to 100%,21 and rates of good clinical outcome after three months ranged from 29%15 to 68%.18
We observed that concomitant IVT enhanced procedural timings significantly and did not result in a higher rate of sICH (5%) compared with other MT studies.31 However, concomitant IVT did not lead to a significantly higher rate of good clinical outcome at 90 days compared with MT and emergency extracranial carotid stenting alone. This finding might be explained by low numbers in the subgroups, which is a drawback of our study. The question about any potential benefit of concomitant IVT in tandem occlusions currently remains unanswered. Nevertheless, we were able to show that it decreases the duration of the procedure, which should translate into a better outcome on a larger scale. The rate of sICH in our study was comparable to published rates of IVT treatment alone in recent randomised trials.8 This is a unique result and has therefore to be replicated in future studies. There are a few variables which might contribute to this finding. The cohort is younger than the average MT patient facing an isolated intracranial occlusion.6–10 This was also observed in a large multicentric retrospective series on tandem occlusions conducted by Behme et al.19 Interestingly, their reported rate of sICH was higher (9%). The reason might be the inhomogeneous antiplatelet regimens in the participating centres. They relied in the majority of cases on intravenous weight adopted glycoprotein IIb/IIIa inhibitors (tirofiban or eptifibatide). None of the participating centres used a half bolus of abciximab. Furthermore, the interruption of any running intravenous rtPA once the guiding catheter is placed correctly in the vasculature has – to the best of our knowledge – not yet been reported, especially not in combination with the administration of a half bolus of abciximab. This more conservative approach might contribute to the relatively low sICH rates in this cohort compared with the literature on tandem occlusions (see comparison in Table 4).11,15,17–23 Notably, the high rate of sICH in the Heck et al. cohort was associated with the use of a standard dose (0.25 mg/kg body weight) of abciximab (4/13 patients [31%] who received abciximab had sICH). In contrast to our approach, they did not administer abciximab in patients with concomitant IVT. The resulting difference from our relatively low rate of sICH might therefore rather be explained by the lower abciximab dosage (0.125 mg/kg body weight) than by the concomitant IVT. Interestingly, this lower dosage did not lead to a higher rate of periprocedural in-stent thrombosis compared to the published series (4/63; 6% vs. 8–17%12,18). Our proposed antiplatelet regimen might be a viable alternative to current practice and should be investigated prospectively.
Table 4.
Studies analysing tandem occlusion treatment with acute carotid artery stenting and stent retriever, ADAPT or Penumbra 1st Generation System–based MT comprising >15 Pt. as of October 2015.
| Study | No. of patients | Initial NIHSS, median (range) | IVT (%) | Final TICI 2b and 3 (%) | sICH (%) | In-hospital mortality (%) | mRS 0–2 90 days (%) | Antiplatelets |
|---|---|---|---|---|---|---|---|---|
| Stampfl et al.15 | 24 | 18 (15–22) | 92% | 63% | 17% | 17% | 29% | 17 Pt. Tirofiban→ASA&CPG |
| 7Pt. ASA+CPG | ||||||||
| Papanagiotou et al.17 | 22 | 17.2 ± 5.3 (M ± SD) | 64% | 63% (TIMI 2/3) | 9% | 14% | 41% | ASA+CPG |
| Steglich-Arnholm et al.18 | 47 | 16 (14–19) | 85% | 87% | 4% | 9% | 68% | Eptifibatide or Abciximab→ASS+CPG |
| Behme et al.19 (multicentric) | 170 | 15 (12–19) | 72% | 77% | 9% | 19% | 36% | Eptifibatide→ASS+CPG or ASA+CPG or Tirofiban→ASA+CPG |
| Cohen et al.20 | 24 | 18 (14–28) | 42% | 79% | 0% | 8% | 54% | ASA+CPG |
| Spiotta et al.21 | 16 | 13.1 ± 3.9 (M ± SD) | 50% | 100% | 6% | 19% | 50% | Abciximab→ASA+CPG |
| Grigoryan et al.22 | 100 | 17.6 ± 5.0 (M ± SD) | 40% | 88% | 6% | N/A | 42% | 49% GP IIb/IIIa inhibitors |
| Fahed et al.23 | 70 | 16 (11.3–19.8) | 74% | 67% | 11% | N/A | 49% | N/A |
| This study | 63 | 14 (1–29) | 52% | 87% | 5% | 8% | 46% | Half bolus Abciximab→ASA+CPG |
ADAPT: A Direct Aspiration First Pass Technique; ASA: acetylsalicylic acid; GP: glycoprotein; CPG: clopidogrel; Pt.: patient; SD: standard deviation; TIMI: Thrombolysis in Myocardial Infarction; N/A: not available.
Spontaneous reperfusion of the intracranial vessel occlusion has been described in the literature in patients with tandem occlusions after emergency stenting of the proximal ICA in 23–27%.16,32 We were able to confirm this finding (24%; antegrade approach subgroup). A prompt antegrade flow restoration in a stent first approach might explain this observation. It remains unclear though whether this contributes to a good clinical outcome, as we saw no TICI 3 results in the antegrade approach subgroup. Consequently, we found a trend towards better clinical 90-day outcome in the retrograde approach subgroup, which in contrast shows 39% TICI 3 recanalization. This finding has been reported in another large series before and justifies further research.33
Our rates of 87% successful recanalization and 46% good clinical outcome with 5% sICH are in line or even better compared to the published literature.11–21 We have summarised the technical and clinical results of all published series comprising more than 15 patients of acute stenting plus MT in tandem occlusions and featuring state-of-the-art MT (stent retriever and/or ADAPT technique) in Table 4. They amount together with our cohort to 536 cases, resulting in an overall rate of sICH of 7%, which is acceptably low for such a procedure in the acute setting.
Limitations
This study has several limitations, including the single-centre retrospective design, its small sample size and lack of a core laboratory analysis for independent grading of the angiographic results. The lack of ASPECTS grading or core volume measurement is a major limitation, reducing the generalisability of our results.
Conclusions
Our single-centre retrospective analysis of emergency stent placement in the extracranial ICA in combination with anterior circulation thrombectomy demonstrated high technical success, reasonable clinical outcomes and acceptable rates of symptomatic intracranial haemorrhage in carefully chosen patients which are triaged interdisciplinary based on clinical and CT imaging criteria. This warrants further study in a randomised prospective trial.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.
Funding
The authors received no financial support for the research, authorship and/or publication of this article.
References
- 1.Grau AJ, Weimar C, Buggle F, et al. Risk factors, outcome, and treatment in subtypes of ischemic stroke: the German stroke data bank. Stroke 2001; 32: 2559–2566. [DOI] [PubMed] [Google Scholar]
- 2.Rubiera M, Ribo M, Delgado-Mederos R, et al. Tandem internal carotid artery/middle cerebral artery occlusion: an independent predictor of poor outcome after systemic thrombolysis. Stroke 2006; 37: 2301–2305. [DOI] [PubMed] [Google Scholar]
- 3.Christou I, Felberg RA, Demchuk AM, et al. Intravenous tissue plasminogen activator and flow improvement in acute ischemic stroke patients with internal carotid artery occlusion. J Neuroimaging 2002; 12: 119–123. [DOI] [PubMed] [Google Scholar]
- 4.Kim YS, Garami Z, Mikulik R, et al. Early recanalization rates and clinical outcomes in patients with tandem internal carotid artery/middle cerebral artery occlusion and isolated middle cerebral artery occlusion. Stroke 2005; 36: 869–871. [DOI] [PubMed] [Google Scholar]
- 5.Labeyrie MA, Turc G, Hess A, et al. Diffusion lesion reversal after thrombolysis: a MR correlate of early neurological improvement. Stroke 2012; 43: 2986–2991. [DOI] [PubMed] [Google Scholar]
- 6.Goyal M, Demchuk AM, Menon BK, et al. Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med 2015; 372: 1019–1030. [DOI] [PubMed] [Google Scholar]
- 7.Campbell BC, Mitchell PJ, Kleinig TJ, et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med 2015; 372: 1009–1018. [DOI] [PubMed] [Google Scholar]
- 8.Berkhemer OA, Fransen PS, Beumer D, et al. A randomized trial of intraarterial treatment for acute ischemic stroke. N Engl J Med 2015; 372: 11–20. [DOI] [PubMed] [Google Scholar]
- 9.Saver JL, Goyal M, Bonafe A, et al. Solitaire™ with the Intention for Thrombectomy as Primary Endovascular Treatment for Acute Ischemic Stroke (SWIFT PRIME) trial: protocol for a randomized, controlled, multicenter study comparing the Solitaire revascularization device with IV tPA with IV tPA alone in acute ischemic stroke. Int J Stroke 2015; 10: 439–448. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Jovin TG, Chamorro A, Cobo E, et al. Thrombectomy within 8 hours after symptom onset in ischemic stroke. N Engl J Med 2015; 372: 2296–2306. [DOI] [PubMed] [Google Scholar]
- 11.Mpotsaris A, Bussmeyer M, Buchner H, et al. Clinical outcome of neurointerventional emergency treatment of extra- or intracranial tandem occlusions in acute major stroke: antegrade approach with wallstent and solitaire stent retriever. Clin Neuroradiol 2013; 23: 207–215. [DOI] [PubMed] [Google Scholar]
- 12.Lockau H, Liebig T, Henning T, et al. Mechanical thrombectomy in tandem occlusion: procedural considerations and clinical results. Neuroradiology 2015; 57: 589–598. [DOI] [PubMed] [Google Scholar]
- 13.Heck DV, Brown MD. Carotid stenting and intracranial thrombectomy for treatment of acute stroke due to tandem occlusions with aggressive antiplatelet therapy may be associated with a high incidence of intracranial hemorrhage. J Neurointerv Surg 2015; 7: 170–175. [DOI] [PubMed] [Google Scholar]
- 14.Maurer CJ, Joachimski F, Berlis A. Two in one: endovascular treatment of acute tandem occlusions in the anterior circulation. Clin Neuroradiol 2015; 25: 397–402. [DOI] [PubMed] [Google Scholar]
- 15.Stampfl S, Ringleb PA, Möhlenbruch M, et al. Emergency cervical internal carotid artery stenting in combination with intracranial thrombectomy in acute stroke. AJNR Am J Neuroradiol 2014; 35: 741–746. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Malik AM, Vora NA, Lin R, et al. Endovascular treatment of tandem extracranial/intracranial anterior circulation occlusions: preliminary single-center experience. Stroke 2011; 42: 1653–1657. [DOI] [PubMed] [Google Scholar]
- 17.Papanagiotou P, Roth C, Walter S, et al. Carotid artery stenting in acute stroke. J Am Coll Cardiol 2011; 58: 2363–2369. [DOI] [PubMed] [Google Scholar]
- 18.Steglich-Arnholm H, Holtmannspötter M, Kondziella D, et al. Thrombectomy assisted by carotid stenting in acute ischemic stroke management: benefits and harms. J Neurol 2015; 262: 2668–2675. [DOI] [PubMed] [Google Scholar]
- 19.Behme D, Mpotsaris A, Zeyen P, et al. Emergency stenting of the extracranial internal carotid artery in combination with anterior circulation thrombectomy in acute ischemic stroke: a retrospective multicenter study. AJNR Am J Neuroradiol 2015; 36: 2340–2345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Cohen JE, Gomori JM, Rajz G, et al. Extracranial carotid artery stenting followed by intracranial stent-based thrombectomy for acute tandem occlusive disease. J Neurointerv Surg 2015; 7: 412–417. [DOI] [PubMed] [Google Scholar]
- 21.Spiotta AM, Lena J, Vargas J, et al. Proximal to distal approach in the treatment of tandem occlusions causing an acute stroke. J Neurointerv Surg 2015; 7: 164–169. [DOI] [PubMed] [Google Scholar]
- 22.Grigoryan M, Haussen DC, Hassan AE, et al. Endovascular treatment of acute ischemic stroke due to tandem occlusions: large multicenter series and systematic review. Cerebrovasc Dis 2016; 41: 306–312. [DOI] [PubMed] [Google Scholar]
- 23.Fahed R, Redjem H, Blanc R, et al. Endovascular management of acute ischemic strokes with tandem occlusions. Cerebrovasc Dis 2016; 41: 298–305. [DOI] [PubMed] [Google Scholar]
- 24.Higashida RT, Furlan AJ, Roberts H, et al. Technology Assessment Committee of the American Society of Interventional and Therapeutic Neuroradiology; Technology Assessment Committee of the Society of Interventional Radiology. Trial design and reporting standards for intra-arterial cerebral thrombolysis for acute ischemic stroke. Stroke 2003; 34: e109–137. [DOI] [PubMed] [Google Scholar]
- 25.Hacke W, Kaste M, Bluhmki E, et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008; 359: 1317–1329. [DOI] [PubMed] [Google Scholar]
- 26.Rha JH, Saver JL. The impact of recanalization on ischemic stroke outcome: a meta-analysis. Stroke 2007; 38: 967–973. [DOI] [PubMed] [Google Scholar]
- 27.Rubiera M, Alvarez-Sabín J, Ribo M, et al. Predictors of early arterial reocclusion after tissue plasminogen activator-induced recanalization in acute ischemic stroke. Stroke 2005; 36: 1452–1456. [DOI] [PubMed] [Google Scholar]
- 28.Nedeltchev K, Brekenfeld C, Remonda L, et al. Internal carotid artery stent implantation in 25 patients with acute stroke: preliminary results. Radiology 2005; 237: 1029–1037. [DOI] [PubMed] [Google Scholar]
- 29.Kappelhof M, Marquering HA, Berkhemer OA, et al. Intra-arterial treatment of patients with acute ischemic stroke and internal carotid artery occlusion: a literature review. J NeuroIntervent Surg 2015; 7: 8–15. [DOI] [PubMed] [Google Scholar]
- 30.Matsubara N, Miyachi S, Tsukamoto N, et al. Endovascular intervention for acute cervical carotid artery occlusion. Acta Neurochir (Wien) 2013; 155: 1115–1123. [DOI] [PubMed] [Google Scholar]
- 31.Behme D, Gondecki L, Fiethen S, et al. Complications of mechanical thrombectomy for acute ischemic stroke-a retrospective single-center study of 176 consecutive cases. Neuroradiology 2014; 56: 467–476. [DOI] [PubMed] [Google Scholar]
- 32.Son S, Choi DS, Oh MK, et al. Emergency carotid artery stenting in patients with acute ischemic stroke due to occlusion or stenosis of the proximal internal carotid artery: a single-center experience. J Neurointerv Surg 2015; 7: 238–244. [DOI] [PubMed] [Google Scholar]
- 33.Lockau H, Liebig T, Henning T, et al. Mechanical thrombectomy in tandem occlusion: procedural considerations and clinical results. Neuroradiology 2015; 57: 589–598. [DOI] [PubMed] [Google Scholar]