Current acute ischemic stroke interventions aim to recanalize occluded arteries to restore cerebral blood flow (1). Intravenous (IV) thrombolysis with tissue type plasminogen activator (tPA) is well documented (1–3). Alternative strategies include entirely endovascular (pharmacological or mechanical) or bridging (IV/pharmacological/ mechanical) therapies (4–6). IV thrombolysis (0.9 mg/kg) is recommended as the first-line therapy for patients with acute ischemic stroke
R. F. Sztajzel1, H. Muller1, L. Sekoranja1, A. Viaccoz1, V. Mendez Pereira2, A. P. Narata2, K. Lovblad2, S. Altrichter2, P. Michel3 1 Department of Neurology, Medical School, University Hospitals of Geneva, Geneva, Switzerland; 2 Department of Radiology, Medical School, University Hospitals of Geneva, Geneva, Switzerland; 3 Department of Neurology, Medical School, University Hospitals of Lausanne, Lausanne, Switzerland
Key words: bridging therapy; intravenous thrombolysis; ischemic stroke; mechanical thrombectomy; proximal acute anterior circulation occlusions R. F. Sztajzel, Neurovascular Unit, Department of Neurology, 24, rue Micheli-du-Crest, 1211 Geneva 14, Switzerland Tel.: +41223728310 Fax: +41223728332 e-mail: [email protected] Accepted for publication September 24, 2014
presenting within 4.5 h of symptom onset (2, 3). However, with IV thrombolysis, chances of successful recanalization are low for proximal large artery occlusions (7–9). For instance, a rate of angiographic recanalization of 9% for T, of 35% for M1, and 54% for M2 segments of the middle cerebral artery (MCA) occlusions has been reported (9). Also, after analysis for stroke severity, the benefit of IV thrombolysis declines with increasing National Institute of Health Stroke Scale (NIHSS) scores (10, 11). Therefore, to improve recanalization in acute stroke, other 329
Sztajzel et al. strategies have been developed. Pharmacological and/or mechanical endovascular approaches have shown higher recanalization rates of up to 71% for T and 84% for the M1 segments of the MCA occlusions (12–17). However, because of potential time delay of primarily endovascular approaches which in turn may tend to minimize their potential advantage, bridging therapies have become an important part of the therapeutic protocols in the daily practice of several stroke centers (5, 6, 18–26). Indeed, bridging therapies consist in a combination of IV/pharmacological and mechanical thrombolysis. In fact, this type of therapy has a theoretical gain by combining rapid treatment initiation with IV tPA to endovascular techniques with higher recanalization rates. Also, it may be used either as rescue treatment in case of unsuccessful IV thrombolysis or as a direct treatment with the endovascular procedure beginning as fast as possible after the start of IV thrombolysis (18–22). Whether a higher recanalization rate reported with endovascular treatment may be translated into a better clinical outcome, it is still a matter of debate. Several clinical trials have explored the role of bridging therapy. Most of these studies used either intra-arterial (IA) tPA or mechanical devices such as Merci (MD) or Penumbra (PD) (13–16). Hence, more recent devices such as the Solitaire stent (StS) have been only marginally included in these studies (24). Also, sites of occlusion assessed radiologically have not been systematically compared side-by-side and evaluated with each therapeutic procedure. The aim of the present work was to compare safety and efficacy of a bridging approach using Solitaire stent (StS) with IV thrombolysis in patients with acute anterior strokes with proximal occlusions treated in two different centers. Patients and methods Patient cohort
All consecutive patients with ischemic anterior strokes admitted within a 4 h 30 min window in two different stroke centers were prospectively collected during the period of 2009–2012 for the bridging therapy and during the period of 2004– 2011 for IV therapy alone.
tory. Only strokes with T, M1, and M2 occlusions confirmed by CT scan angiography (CTA) were considered for this analysis. Assessments of the occlusion site on CTA were performed in each center by an experienced neuroradiologist, unaware of the clinical data except of the ischemic event’s side. Hemorrhagic complications were defined according to ECASS II criteria (27). IV therapy
In one center, the preferred treatment was IV standard thrombolysis alone, using alteplase 0.9 mg/kg with a bolus of 10% (during 1 min). Bridging therapy
In the other center, the preferred approach was IV therapy during 30 min. A dose of tPA of 0.6 mg/ kg with a bolus of 15% (during 1 min) was administered during the first 30 min for all patients. In case of absence of clinical improvement defined by a reduction of the NIHSS of ≥4 points and a total NIHSS of <8, mechanical thrombectomy using StS was performed. Whenever needed, additional alteplase was used intra-arterially with a maximum dose of 22 mg. The preparation of the endovascular intervention was initiated immediately after the detection of an occluded artery on CTA. After the start of tPA infusion, all patients were transferred to the angiographic suite. Patients underwent sedation or general anesthesia according to clinical status and stroke severity. In patients with a risk of aspiration, loss of consciousness, or severe aphasia with poor cooperation, general anesthesia was preferred. An 8-F balloon guiding catheter was placed into the proximal ICA. The site of occlusion was reached using a 18 microcatheter system (Rebar 18; Covidien Neurovascular, Irvine, CA, USA) and a 14 microguidewire. After passage of the clot and placement of the microcatheter distally, the correct position was verified by an additional angiogram obtained with microcatheter injection. After the microcatheter was pulled back, the stent retriever was deployed fully, followed by control angiography to evaluate successful deployment. Then, after approximately 5 min, the unfolded device was pulled back with continuous aspiration from the guiding catheter to prevent embolization of the migrating thrombus.
Imaging analysis and patients selection
Imaging evaluation excluded patients with signs of intracranial hemorrhage, arteriovenous malformation, or aneurysm, early ischemic changes larger than one-third of the middle cerebral artery terri330
Assessment of angiographic recanalization
We used the thrombolysis in cerebral infarction score (TICI) with TICI grade 0 defined as no perfusion, grade 1 defined as perfusion past the
Bridging versus intravenous thrombolysis initial obstruction but with limited distal branch filling and with little or slow distal perfusion, grade 2a defined as only partial filling of the entire vascular territory, grade 2b defined as complete filling of all of the expected vascular territory but with a slower filling than normal, and grade 3 defined as full perfusion with complete filling of all distal branches (28). Endpoints
Endpoints of the study were clinical outcome according to modified Rankin scale at 3 months and mortality. Statistical analysis
For statistical evaluation, t- and chi-square tests were used. A multivariate logistic regression analysis was performed with a selection on the basis of variables with univariate P values of <0.05. Statistical analysis was performed by means of Medcalc program.
differences regarding age and NIHSS at admission were observed. Time to IV therapy was slightly more elevated in the bridging group, but the difference did not reach significance: 150 min (mean) in the bridging and 144 min (mean) in IV group (P = NS). Sites of occlusions
There were 11 (17%) and 24 (15%) carotid T, 42 (67%) and 99 (61%) M1, and 10 (16%) and 40 (25%) M2 occlusions (Table 2). Revascularization percentage and TICI classification
The recanalization rates with StS were the following: all patients presented a TICI 0 score at the beginning of the angiography; at the end of the procedure, there were 1 (1.5%) TICI 0, 2 (3%) TICI 1, 11 (17%) TICI 2a, 8 (13%) TICI 2b, and 41 (65%) TICI 3. The recanalization rates according to sites of occlusion are given in Table 2. Sedation only, without general anesthesia, could be performed in 44 patients (70%).
The local ethics committees approved the study. Results Patient baseline variables
Sixty-three patients were included in the bridging and 163 in the IV group. Their main characteristics are summarized on Table 1. No significant Table 1 Baseline characteristics of the patients
Age (mean) Male High blood pressure Diabetes Hyperlipemia Tobacco CAD Atrial fibrillation Blood sugar at admission (mean) Blood pressure at admission SAP (mean) DAP (mean) Mean NIHSS at admission Mean OT IV* Mean time between end of IV and beginning of IA therapy CAD, coronary heart disease. *Onset time to IV thrombolysis.
Symptomatic intracranial hemorrhages (SICH) were documented in 6.3% (n = 4) vs 3.7% (n = 6) in the bridging and in the IV group, respectively (P = 0.32). There were more asymptomatic intracranial hemorrhages in the bridging (35%, n = 22) than in the IV group (23%, n = 37); the difference however did not reach statistical significance (P = 0.1). Similar rates of mortality were observed at 3 months (14% vs 18%, respectively, in the bridging and the IV group, P = 0.32). Clinical outcome at 3 months
At 3 months, 46% (n = 29) of the patients treated in the bridging group had a mRS of 0–1 as compared to 23% (n = 38) of those treated in the Table 2 Sites of occlusion and recanalization rates IV group N = 163 (%)
Figure 1. Modified Rankin scores at 3 months in combined and IV groups.
Figure 3. Significant better outcome at 3 months according to recanalization rate in the bridging compared to the IV group.
did not observe any particular association regarding clinical outcome and time between end of IV and beginning of endovascular therapy. Results of the patients treated only intravenously during the same period in the bridging center
Figure 2. Proportion of good outcome at 3 months according to site of occlusion: comparison between bridging and IV groups.
IV group (P < 0.001; Fig. 1). This was also valid for all sites of occlusion (Fig. 2). Further, no significant difference regarding mRS 0–2 was observed between the two groups, as there were, respectively, 35 (56%) in the bridging and 79 (48%) in the IV group (P = 0.2). For the prediction of good clinical outcome, we included the following variables: age, sex, serum level of glucose and blood pressure at admission, onset-toIV treatment, baseline NIHSS score, and use of IV or bridging therapy. In a logistic regression model including the above-mentioned parameters, only NIHSS at admission and bridging therapy resulted to be independent predictors of good outcome (respectively, OR, 0.88; 95% CI, 0.82– 0.94; and P = 0.001, and OR, 1.7; 95% CI, 1.2– 2.2; and P = 0.0018). We found in our bridging cohort a significant correlation between recanalization rate and good outcome. As shown on Fig. 3, only patients with a TICI score of ≥2b presented a mRS between 0 and 1 at 3 months (P = 0.009). Among those patients presenting a TICI score of less than TICI 2b, there were only 2 (14%) with a favorable mRS of 2. Lastly, we 332
In the center using bridging therapy, 73 patients were treated only intravenously during the same period. Of these, 32 presented proximal occlusions, 1 with T (3%), 11 with M1 (34%), and 20 with M2 ones (63%). The mean NIHSS within this group of patients was of 12.4. As these patients improved clinically after 30 min of IV thrombolysis, the treatment was continued over 1 h. Thirty-eight percent of the patients achieved a good outcome (mRS 0–1) and 55% a favorable one (mRS 0–2). This further explains the lower number of M2-occlusions in the bridging group (Table 1), as 63% of patients with M2-occlusions improved clinically after 30 min of IV thrombolysis and did not require additional endovascular treatment. No correlations were found in this group between time to IV treatment and clinical outcome. Discussion
Our study showed, in a two-center comparison of bridging approach with IV thrombolysis, that patients treated with bridging therapy were more likely to have minimal or no deficit at all at 3 months as compared to IV treated group. In a logistic regression model including the parameters age, sex, serum level of glucose, blood pressure at admission, onset-to-IV treatment, baseline NIHSS score, and use of IV or bridging therapy, only NIHSS at admission and bridging therapy resulted to be independent predictors of good
Bridging versus intravenous thrombolysis outcome (respectively, OR, 0.88; 95% CI, 0.82– 0.94; and P = 0.001, and OR, 1.7; 95% CI, 1.2–2.2; and P = 0.0018). In the bridging group, 78% of the patients could be recanalized with a TICI score of 2b or 3 (Table 2). Also, a significant correlation between the recanalization rate and good outcome was present in our bridging cohort. Indeed, as shown on Fig. 3, only patients with a TICI score of ≥2b presented a mRS between 0 and 1 at 3 months (P = 0.009). No difference between the two groups was observed regarding symptomatic intracranial hemorrhage or mortality. Until now, only a few studies have compared the efficacy and safety of bridging therapy with IV thrombolysis. The REcanalisation using Combined intravenous Alteplase and Neurointerventional ALgorithm for acute Ischemic StrokE (RECANALISE) study evaluated patients receiving bridging therapy with historic IV tPA patients with confirmed arterial occlusion (19). Although the recanalization rate was higher in the endovascular rescue group, the study did not demonstrate a significant functional improvement in favor of the bridging group. The recently published IMS III trial randomly assigned eligible patients who received IV tPA within 3 h after symptom onset to receive additional endovascular therapy or IV tPA alone (24). No difference between the two treatment protocols was found with respect to favorable outcome at 90 days (40.8% with endovascular therapy and 38.7% with IV tPA). Conversely, in another recent study, Rubiera and colleagues compared bridging therapy and IV thrombolysis using a case–control approach and found not only a significantly higher rate of complete recanalization in the bridging group, but also a better clinical evolution at 3 months (22). Lastly, a recent metaanalysis published by Mazighi and coworkers, including 15 studies using bridging therapy, displayed a pooled estimate for recanalization rate and for favorable clinical outcome of, respectively, 69.6% and of 48.9%. Also, the comparison with IV treatment alone in eight control groups demonstrated a superiority of bridging therapy with respect to favorable outcome (OR, 2.26; 95% CI, 1.16–4.40). Moreover, shorter mean time to IV treatment was associated with greater recanalization rates (20). One important and common point among all the above-mentioned studies is the primary use of intra-arterial (pharmacological) tPA or of first generation mechanical devices such as the Merci retriever or Penumbra System. Yet these devices did not show the expected rates of clinical improvement despite achieving high recanalization rates. This
aspect is clearly illustrated in the Penumbra pivotal trial with 82% of partial or complete recanalization but only 25% of functionally independent patients (16). However, newer devices such as StS appear to be superior. Indeed, a recent study showed that patients treated with StS presented not only higher recanalization rates but also a better 3-month neurological outcome in comparison with those patients treated with the Merci retriever (29). We found a significant difference between bridging therapy and IV thrombolysis for the mRS of 0–1, but not for mRS of 0–2. There is one important reason, in our opinion, which could at least partially explain these findings. As mentioned in the results section, in the center with combined treatment, 73 patients were treated only intravenously during the same period as they improved clinically after 30 min. The number of M2-occlusions was important in this group of patients and explains also why this site of occlusion was less represented in the bridging group. These findings also support earlier reports showing that IV thrombolysis alone may be able to recanalize occluded M2-segments in about 50% of the cases (9). The proportion of patients with favorable outcome (mRS 0–2) was surprisingly high in the IV group compared to previous findings. In the study reported by Rubiera and colleagues, there were only 14.9% of the patients treated with IV thrombolysis presenting functional independency (mRS 0–2) at 3 months (22). Also in another recent study, Mattle and coworkers showed, among 112 acute ischemic stroke patients exhibiting a hyperdense sign of the middle cerebral artery on CT scan, that favorable outcome was more frequent after IA (n = 29, 53%) than after IV thrombolysis (n = 13, 23%; P < 0.001) (29). Not only the stroke severity may account for this difference as the mean NIHSS was of 20 and 17.5, respectively, in Rubiera’s and Mattle’s studies but also the time to therapy was longer in these trials, respectively, mean 182 and 156 min. It is debatable whether the bridging approach should be applied as a rescue treatment after lack of result to IV therapy or as a direct endovascular treatment started as quickly as possible after initiation of IV thrombolysis. Rescue therapy offers eventually the advantage to avoid an endovascular procedure in patients responding favorably to IV treatment alone. It must be mentioned however that there is a very low rate of complications when angiography is performed in patients having already recanalized with IV therapy (24). A recent study demonstrated that treatment with 333
Sztajzel et al. IV tPA before endovascular therapy compared with endovascular therapy alone resulted in a significantly higher rate of neurological recovery at 3 months (IV tPA, 66%; no IV tPA, 42%; P < 0.01) (30). Accordingly, as clot-lysis with IV tPA may require some time, endovascular therapy should not start too early. On the other hand, beginning of endovascular treatment must not be retarded as it has been shown that clinical outcome following angiographically successful reperfusion is significantly time dependent (21). Moreover, rapid arterial recanalization within 30 min during IV thrombolysis is associated with a better short-term clinical outcome as compared to later recanalization (32) Therefore, as time to start angiography takes usually at least 30 min, rescue therapy should be performed in our opinion, at this point rather than after 60 min. Whether the initial IV tPA dosage should be 0.6 or 0.9 mg/kg before endovascular therapy remains controversial. One meta-analysis published by Georgiadis et al. (33) suggested that 0.9 mg/kg IV tPA before IA thrombolysis was safe and associated with higher recanalization rates and better functional outcome. On the contrary, in another more recent meta-analysis, no differences were found between theses 2 dosages with respect to recanalization, functional outcome, mortality, or symptomatic intracranial hemorrhages (19). Our study does not contribute to highlight this point as none of our patients in the bridging group received the total amount of 0.9 mg/kg IV tPA. Nevertheless, for some patients, fairly good results could be achieved regarding recanalization and functional outcome with the administration of only 0.6 mg/kg IV tPA before endovascular procedure, thus justifying the use of the low dosage. Even if the data were prospectively collected, the main limitation of our study is its retrospective nature. The fact that the patients were recruited in two different centers could potentially also influence the results although it should be mentioned that besides their different thrombolytic treatment modalities, the two stroke centers had a very similar standardized patient management care and were geographically close.
as primary use in the combined group are needed. Acknowledgements The study was funded by the Swiss Heart Foundation.
Conﬂict of interest None.
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Our results suggest that patients treated with combined therapy were more likely to have minimal or no deficit at all at 3 months as compared to the IV treated group. Further randomized studies comparing the two treatment modalities and including mechanical thrombectomy with StS 334
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Stroke with tandem occlusion within the anterior circulation presents a lower probability of recanalization and good clinical outcome after intravenous (IV) thrombolysis than stroke with single occlusion. The present study describes the impact of end
Major anterior circulation ischemic strokes caused by occlusion of the distal internal carotid artery or proximal middle cerebral artery or both account for about one third of ischemic strokes with mostly poor outcomes. These strokes are treatable by