Abstract
Background
We investigated the properties and effects of 5 mechanical thrombectomy procedures in patients with acute ischemic stroke. The relationships between the type of procedure, the time required, the success of recanalization, and the clinical outcome were analyzed.
Material/Methods
This prospective comparative analysis included 500 patients with acute ischemic stroke and large-vessel occlusion. We compared contact aspiration thrombectomy (ADAPT, n=100), stent retriever first line (SRFL, n=196), the Solumbra technique (n=64), mechanical thrombectomy plus stent implantation (n=81), and a combined procedure (n=59).
Results
ADAPT provided shorter procedure (P<0.001) and recanalization times (P<0.001) than the other techniques. Better clinical outcome was achieved for ischemia in the anterior circulation than ischemia in the posterior fossa (P<0.001). Compared to the other techniques, patients treated with ADAPT procedure had increased odds of achieving better mTICI scores (P=0.002) and clinical outcome (NIHSS) after 7 days (P=0.003); patients treated with SRFL had increased odds of achieving better long-term clinical status (3M-mRS=0–2; P=0.040). Patients with SRFL and intravenous thrombolysis (IVT) had increased odds of better clinical status (3M-mRS=0–2; P=0.031) and decreased odds of death (P=0.005) compared to patients with SRFL without IVT. The other treatment approaches had no additional effect of IVT. Patients with SRFL with a mothership transfer had increased odds of achieving favorable clinical outcome (3M-mRS) compared to SRFL with the drip-and-ship transfer paradigm (P=0.015).
Conclusions
Our results showed that ADAPT and SRFL provided significantly better outcomes compared to the other examined techniques. A mothership transfer and IVT administration contributed to the success of the SRFL approach.
MeSH Keywords: Stroke, Thrombectomy, Thrombolytic Therapy
Background
The beginnings of mechanical thrombectomy can be traced to 1998, when the Amplatz Goose Neck extraction loop was first used to extract a thrombus from the brain. This technique was successfully used in Gothenburg [1]. Since then, other devices were developed, including the Neuronet (Mayer 2002), the InTime, and the EnSnare. A breakthrough was made with the helical loop „corkscrew” (Concentric Medical Mountain View, CA). In the MERCI trial, the extractor was used together with a balloon-occlusive guiding catheter [2,3]. The first stent retriever was the Solitaire (EV3; then Medtronic Neurovascular, Irvine, CA). In 2012, comparative studies were conducted to compare the MERCI to the Solitaire (SWIFT trial) [4] and Trevo (TREVO II study) stent retrievers [5].
In March 2013, 3 randomized trials were published, and none showed that endovascular treatments provided any benefit over standard therapy, including intravenous thrombolysis (IVT). In the MR RESCUE trial, the MERCI Retriever and Penumbra System were tested and compared to standard treatment [6]. In the IMS-III trial, patients were treated with IVT and randomized into the following 2 groups within 3 h: in the first group, IVT was followed by a subsequent mechanical thrombectomy; in the second group, IVT was not followed by endovascular treatment [7]. In the SYNTHESIS trial, patients were treated with IVT alone or IVT followed by intra-arterial thrombolysis, mechanical thrombus disruption, or thrombus retrieval within the therapeutic window of 4.5 h [8].
Five new randomized trials published in 2015 successfully showed the benefit of endovascular treatment: (1) The MR CLEAN – Multicenter Randomized Trial of Endovascular Treatment for Acute Ischemic Stroke in the Netherlands was published in January 2015. The study included 500 patients, and convincingly demonstrated superiority of mechanical thrombectomy by stent retriever together with standard treatment (89% IVT) compared with standard treatment (90% IVT alone) [9]. (2) The ESCAPE trial, which was focused on proximal occlusion of the arteries in the anterior circulation within the therapeutic window of 12 h from the onset of symptoms. They compared IVT followed by endovascular treatment versus a standard IVT treatment [10]. (3) The Solitaire Retriever Study (SWIFT-PRIME) was conducted in 39 centers in the USA and Europe, and it included 196 patients [11]. (4) The EXTEND-IA study was conducted in Australia and New Zealand and they tested whether better imaging technologies, new intervention products, and earlier interventional performance could improve clinical results [12]. (5) The REVASCAT trial was a randomized study that included 206 patients, performed in Catalonia, Spain [13]. These 5 studies changed the approach to acute ischemic stroke and led to the ESO-ESMINT-ESNR-EAN consensus statement, published in 2016 [14].
Blood clot aspiration was originally performed in lower limbs peripheral arterial interventions and manual aspiration was applied. Briefly, 4–8 F aspiration catheters were inserted close to the thrombus; then, the thrombus was simply sucked out by applying vacuum manually with a syringe [15]. In 2009, Penumbra Systems (Almeda, CA, USA) launched aspiration catheters for use in the brain. The first results, presented in 2009 in The Penumbra Pivotal Stroke Trial, showed successful revascularization, with high thrombolysis in myocardial infarction – TIMI score (2–3), in 82% of patients, a low modified Rankin Scale – mRS (0–2) in 25% of patients, and 33% mortality [16]. Later results were more encouraging, with a low mRS (0–2) in 43% of patients [17].
Later, 2 techniques were introduced: the forced aspiration suction thrombectomy (FAST) in 2011, and a direct aspiration first-pass technique (ADAPT) in 2014 [18,19]. These catheters had a smaller lumen than those of the later Penumbra catheters (5MAX and 3MAX) and the aspiration was performed by hand with a syringe. The use of occlusive balloon guiding catheters was demonstrated in the SWIFT and SWIFT-PRIME studies, where extractions were performed with larger stent retrievers. Their benefit was that fragmentation and distal embolization of the aspirated thrombus was inhibited when blocking the flow through the internal throat of the guiding catheter. The ADAPT technique uses a rapid, distal approach and newer catheters (ACE64 or ACE68) with a larger internal lumen. The aspiration is performed with a dedicated vacuum pump that provides continuous suction. A 3MAX aspiration catheter is often used for distal access to the M2-MCA, A2-ACA, and P2-PCA branches. Various aspiration catheters with various internal lumen parameters are currently available for use in aspiration techniques [20].
Currently, a combined technique is increasingly being used because it has the advantages of both the FAST and ADAPT techniques. The combination is based on the use of a large internal diameter aspiration catheter (Penumbra ACE64, ACE68) and stent retrievers, like Solitaire FR, pREset, Catch, and Tiger triever. Concurrent aspirations during thrombus extraction can reduce fragmentation and distal embolization during mechanical thrombectomy [21,22]. In September 2016, the results of the THERAPE study were published [23], which evaluated the Penumbra aspiration system combined with IVT compared to IVT administration alone in the control group. The ASTER study recently presented results on their comparison between the primary use of aspiration versus a stent retriever [24,25].
The present study investigated the properties and effects of these 5 types of mechanical thrombectomy procedures in patients with acute ischemic stroke. The relationships between the type of procedure, the time required for the procedure, the success of recanalization, and the clinical outcome were analyzed.
Material and Methods
Study population and data collection
This prospective study included 500 patients with acute ischemic stroke and large-vessel occlusion (LVO) who were treated with contact aspiration technique (ADAPT) or first-pass stent retriever (SRFL) or aspiration plus extraction technique (Solumbra) or combined procedure (CP) with mechanical thrombectomy plus angioplasty and/or stenting. We performed a comparative study on the efficacy and safety of these techniques. We recorded the times from the onset of stroke to the hospital arrival (onset-to-door), from onset to the insertion of the needle for IVT (onset-to-needle), from the hospital door to the angiography suite arrival (door-to-DSA), and from the onset of stroke to recanalization of the target blood vessel (onset-to-recanalization).
Early ischemic changes and collateral circulation were assessed with the e-Alberta stroke program for early computed tomography (CT) ischemic score (e-ASPECTS) and with computed tomography angiography (CTA) localization of the LVO. We also recorded data from the neurointerventional procedure (modified thrombolysis in cerebral infarction score [mTICI], type of procedure, and procedure duration). Neurological clinical status was evaluated with the National Institutes of Health Stroke Scale score (NIHSS) obtained at patient admission, after 24 h, and on day 7, and with the modified Rankin Scale after 3 months (3M-mRS). Outcome safety data included symptomatic or non-symptomatic intracerebral hemorrhage (ICH) and death (3M-mRS=6). Safety outcomes were compared among the examined treatment methods.
Eligibility criteria
Inclusion criteria
Age 18 and older (i.e., patients must have had their 18th birthday).
NIHSS ≥8 at the time of neuroimaging.
Presented symptoms or symptoms persisted within 6 h of obtaining a groin puncture.
Neuroimaging demonstrated an LVO.
Stroke appropriately treated with the ADAPT approach or conventional first-line stent retriever approach or combined procedure.
Pre-event mRS score=0–1.
CT/CTA eligibility confirmed.
Exclusion criteria
Patient admission later than 6 h from symptom onset.
NIHSS <4 at the time of neuroimaging.
Absence of LVO on non-invasive imaging.
Presence of an existing or pre-existing large-territory infarction.
Chronic LVO in the symptomatic territory.
Excessive vascular access tortuosity that was likely to result in unstable access platform.
Severe contrast allergy or absolute contraindication to iodinated contrast.
-
Head CT or MRI scan exclusion criteria:
– Subarachnoid hemorrhage (SAH), intracerebral hemorrhage (ICH),
– High-density lesion consistent with hemorrhage of any degree,
– Significant mass effect with midline shift, core infarct lesion volume >50 cc,
– Large (>1/3 of the middle cerebral artery) regions of clear hypodensity on the baseline CT scan or e-ASPECTS <5,
– Sulcal effacement and/or loss of grey-white differentiation alone were not taken as contraindications for treatment.
Interventions
Patients with acute ischemic stroke were treated according to the ESO-EAN-ESMINT recommendations for the LVO [14]. Patients eligible for IVT received it, according to the guidelines, after exclusion of ICH. After the LVO confirmation, patients were transported from the primary stroke center (with the drip-and-ship paradigm) either to the neurointerventional department for an acute revascularization procedure, or directly to the mothership comprehensive stroke center. Mechanical thrombectomies that were performed with a stent retriever, Penumbra aspiration device, or a combined technique were conducted at the University Hospital Ostrava, Interventional Neuroradiology and Angiology Department. A GE-Innova IGS 630 biplane system (GE Healthcare, Buc, France) was used to image the 3D-XRA angiography reconstructions during and after the stroke procedure. The type of anesthesia used was recorded during the procedure (e.g., local anesthesia, intravenous analgosedation with a laryngeal mask, or general anesthesia). Brain vessels were accessed with a Flexor 6–7 F/90 cm guiding sheath (Cook Medical, Bjaeverskov, Denmark) or Terumo Destination guiding catheter (Terumo Medical Corp., Elkton, MD, USA). Large-vessel occlusions (LVOs) were recanalized with the ADAPT first-pass technique using the Prowler Select Plus microcatheter (Codman & Shurtleff, Inc., Raynham, MA) over several types of 0.014” microwires. The aspiration catheter was pushed into direct contact with the thrombus. For the contact aspiration technique, we used ACE64, ACE68, and 3MAX Penumbra aspiration systems (Penumbra, Inc., Alameda, CA) with the original suction pump. When the ADAPT technique failed due to complex tortuosity or atherosclerosis in the brain supplying vessel, a stent retriever was used as the rescue technique. For the SRFL mechanical thrombectomy, we used a pREset thrombectomy device (Phenox GmbH, Bochum, Germany), Catch retriever (Balt Extrusion, Montmorency, France), or Solitaire stent retriever (Medtronic, Dublin, Ireland). When necessary, a combination of procedures was used, with either extracranial or intracranial stent implantation and extracranial or intracranial angioplasty, in cases of tight residual stenosis.
Statistical analyses
Numerical variables are described with the median and interquartile range (IQR). Graphical representations (with boxplots) were used to explore the structure of selected variables and to facilitate comparisons among several groups of interest. The Kruskal-Wallis test was used to identify significant differences among the examined groups. We analyzed the relationship between 2 categorical variables with contingency tables, 100% stacked bar charts, and the chi-square test of independence. Finally, we used the odds ratio (OR) to evaluate the association between the presence of a risk factor and the outcome. All statistical analyses were performed with maximum available data.
Results
The cohort comprised 500 patients, including 269 men (54%) and 231 women (46%), with a median age of 69 years (IQR: 61–75 years), with LVO and acute ischemic stroke symptoms. All patients underwent a mechanical thrombectomy with one of the following techniques: aspiration thrombectomy, first line procedures, with a Penumbra device (ADAPT, 100 patients); stent retriever, first-line procedures (SRFL, 196 patients); Solumbra technique (64 patients); mechanical thrombectomy and stent implantation (MT + stent, 81 patients); or a combined procedure (CP, 59 patients).
The degree of stroke-related disability/dependence, based on the 3M-mRS, was not significantly different between sexes (P=0.693). However, on average, 3M-mRS scores indicated that better clinical outcome was achieved by significantly younger patients (P<0.001). Table 1 describes the distribution (occurrence) of selected risk factors, expressed in terms of absolute and relative frequencies (%). We did not find a significant relationship between the 3M-mRS score and the presence of hypertension, diabetes mellitus, arrhythmia, or hyperlipidemia (P=0.335, P=0.215, P=0.196 and P=0.169, respectively). However, better mTICI scores (2–3) were significantly related to better 3M-mRS clinical outcomes (P<0.001). We observed no significant difference in outcomes (P=0.316) among patients who received different types of anesthesia for mechanical thrombectomy procedures (Figure 1).
Table 1.
Patient demographics and medical history. Demographics and medical history of patients with large-vessel occlusion in acute ischemic stroke that were treated with different mechanical thrombectomy techniques.
| Variable | ADAPT (n=100) | SRFL (n=196) | Solumbra (n=64) | MT+stent (n=81) | CP (n=59) |
|---|---|---|---|---|---|
| Gender (Female) | 47 (47) | 106 (54) | 30 (47) | 32 (40) | 16 (27) |
| Hypertension | 82 (82) | 157 (80) | 53 (85) | 58 (72) | 48 (83) |
| Diabetes mellitus | 24 (24) | 39 (20) | 10 (16) | 12 (15) | 16 (28) |
| Arrhythmia | 62 (62) | 107 (55) | 39 (62) | 27 (33) | 10 (18) |
| Hyperlipidemia | 58 (58) | 75 (38) | 32 (50) | 25 (31) | 27 (46) |
| IVT (yes) | 74 (74) | 131 (67) | 50 (78) | 53 (65) | 41 (70) |
| (yes, Mothership) | 58 (58) | 70 (36) | 37 (58) | 30 (37) | 24 (41) |
| (yes, Drip-and-ship) | 16 (16) | 61 (31) | 13 (20) | 23 (28) | 17 (29) |
| Antithrombotics (yes) | 52 (52) | 85 (43) | 33 (52) | 26 (32) | 18 (30) |
| Anesthesia (analgosedation) | 35 (35) | 44 (22) | 22 (34) | 13 (16) | 9 (15) |
| (general) | 53 (53) | 93 (47) | 33 (52) | 42 (52) | 42 (71) |
| mTICI (2–3) | 98 (98) | 170 (87) | 56 (88) | 72 (89) | 51 (86) |
| 3M-mRS (0–2) | 44 (44) | 87 (44) | 16 (25) | 27 (33) | 15 (25) |
| Mortality | 21 (21) | 40 (21) | 13 (20) | 14 (17) | 14 (24) |
Values represent the absolute frequency and relative frequency (%), in parentheses.
Figure 1.
Clinical outcome comparison by the type of anesthesia. Comparison of clinical outcomes for patients treated with different types of anesthesia. Clinical outcome was the degree of stroke-related disability/dependence, based on the 3M-mRS score (color-coded: 0=no symptoms, 6=death).
Comparisons of important time variables are shown in Figure 2 and Table 2. Patients treated with the ADAPT technique had significantly shorter procedure times (P<0.001) and recanalization times (P<0.001) compared to the other recanalization methods. The shorter time for the ADAPT procedure was due to its simple, rapid set-up for preparing the neurointerventional procedure and repeated aspiration runs.
Figure 2.
Selected time variables by the type of procedure. Comparisons of time required for different procedures. (A) Total procedure durations (P<0.001). (B) Recanalization times (P<0.001).
Table 2.
Descriptive characteristics of selected time variables.
| Technique | Total procedure duration (min) | Time of recanalization (min) |
|---|---|---|
| ADAPT | 35 (25–40) | 180 (152–225) |
| SRFL | 45 (30–60) | 220 (180–271) |
| Solumbra | 60 (50–71) | 225 (175–258) |
| MT+stent | 60 (50–80) | 242 (182–310) |
| CP | 70 (55–88) | 270 (220–320) |
Procedural times for different types of mechanical thrombectomy techniques. Values are the median (IQR).
We also analyzed the location of the LVO. The right hemisphere was affected in 206 cases, the left hemisphere in 232 cases, and an LVO in the posterior fossa circulation was observed 62 times. We analyzed the distribution of specific therapeutic approaches used in the different affected brain areas (Figure 3, Table 3). We found no significant differences in the use of different procedures for the different brain areas (P=0.297). Approximately 60% of procedures were performed with ADAPT or SRFL, regardless of the affected brain area.
Figure 3.
Distribution of the types of procedure by the affected area. Distribution of the types of procedure used in 3 brain areas affected by large-vessel occlusions.
Table 3.
Contingency table for the affected brain area and the type of procedure. Numbers of procedures used in 3 different affected brain areas.
| Brain area | ADAPT | SRFL | Solumbra | MT +stent | CP | Total |
|---|---|---|---|---|---|---|
| Right hemisphere | 44 | 84 | 21 | 34 | 23 | 206 |
| Left hemisphere | 43 | 87 | 40 | 35 | 27 | 232 |
| Posterior fossa | 13 | 25 | 3 | 12 | 9 | 62 |
| Total | 100 | 196 | 64 | 81 | 59 | 500 |
However, the clinical outcome of mechanical thrombectomy procedures differed according to the stroke location. Procedures performed in the anterior (right hemisphere) circulation achieved significantly better clinical outcomes than those performed in the posterior fossa (P<0.001; Figure 4). The poor clinical outcome (3M-mRS=6 in 48%) in the posterior fossa was influenced by the higher NIHSS scores in that patient group at the time of hospital admission (NIHSS ≥15 in 63%). Patients transferred with drip-and-ship paradigm from other centers or directly admitted to a mothership center were typically intubated and put under general anesthesia.
Figure 4.
Clinical outcome comparison by the affected brain area. Clinical outcomes among patients treated for large-vessel occlusions in different brain areas. Clinical outcome was the degree of stroke-related disability/dependence, based on the 3M-mRS score (color-coded: 0=no symptoms, 6=death).
We analyzed the relationship between the type of endovascular treatment procedure and clinical outcome. Outcomes were evaluated with the NIHSS (at 24 h and 7 days after the procedure) and with the 3M-mRS (Figure 5). Significant differences between groups were observed in the NIHSS evaluated 7 days after the endovascular procedure (P=0.004). However, from a practical point of view, patients achieved better 3M-mRS scores with the ADAPT and SRFL techniques compared to the other procedures (Figure 5C).
Figure 5.
Clinical outcome comparison by the type of procedure. Clinical outcomes in patients with acute ischemic stroke, treated with different mechanical thrombectomy procedures. Outcomes were measured as (A) NIHSS (color-coded: 0=normal function, 42=severe impairment) after 24 h; (B) NIHSS after 7 days; and (C) 3M-mRS (color-coded: 0=no symptoms, 6=death).
Patients treated with ADAPT had significantly increased odds of achieving better perfusion (high mTICI scores; P=0.002) and better clinical outcome (low NIHSS scores after 7 days; P=0.003) compared to those treated with other techniques (Table 4). Patients treated with SRFL had significantly increased odds of achieving a better long-term clinical status (3M-mRS=0–2; P=0.040) than those treated with the other techniques. On the other hand, with a combined procedure, where several devices were used for LVO recanalization, patients had significantly lower odds of achieving a favorable 3M-mRS score compared to those treated with the other techniques (P=0.035). However, the type of procedure did not significantly affect the death rate (3M-mRS=6).
Table 4.
Comparison of the types of procedure. Odds of achieving favorable outcomes or death (3M-mRS=6) with the different types of procedures.
| mTICI (2–3) OR (95% CI) | P | |
|---|---|---|
| Procedure | ||
| ADAPT | 7.41 (1.76; 31.15) | 0.002 |
| SRFL | 0.75 (0.41; 1.38) | 0.362 |
| Solumbra | 0.58 (0.25; 1.32) | 0.189 |
| MT+stent | 1.00 (0.44; 2.24) | 0.993 |
| CP | 0.54 (0.23; 1.25) | 0.144 |
| NIHSS after 7 days (<10) OR (95% CI) | P | |
| Procedure | ||
| ADAPT | 2.04 (1.27; 3.30) | 0.003 |
| SRFL | 1.07 (0.73; 1.55) | 0.740 |
| Solumbra | 0.69 (0.40; 1.18) | 0.175 |
| MT+stent | 0.73 (0.45; 1.18) | 0.197 |
| CP | 0.69 (0.40; 1.20) | 0.189 |
| 3M-mRS (0–2) OR (95% CI) | P | |
| Procedure | ||
| ADAPT | 1.42 (0.90; 2.25) | 0.128 |
| SRFL | 1.48 (1.02; 2.16) | 0.040 |
| Solumbra | 0.55 (0.30; 1.02) | 0.055 |
| MT+stent | 0.80 (0.48; 1.34) | 0.398 |
| CP | 0.52 (0.28; 0.96) | 0.035 |
| 3M-mRS (6) OR (95% CI) | P | |
| Procedure | ||
| ADAPT | 1.06 (0.61; 1.83) | 0.838 |
| SRFL | 0.94 (0.60; 1.47) | 0.786 |
| Solumbra | 1.10 (0.57; 2.13) | 0.784 |
| MT+stent | 0.80 (0.42; 1.49) | 0.474 |
| CP | 1.26 (0.66; 2.42) | 0.484 |
Values are odds ratio (OR) and 95% confidence intervals (95% CI); P-values were evaluated with the chi-square test of independence.
We further investigated whether an IVT prior to the mechanical thrombectomy procedure was related to clinical outcome and the occurrence of symptomatic ICH after different endovascular procedures (Table 5). Patients treated with SRFL and IVT had significantly higher odds of achieving a favorable clinical status (3M-mRS=0–2) than patients treated with SRFL without IVT (P=0.031). Also, patients treated with SRFL and IVT had significantly decreased odds of death compared to patients with SRFL without IVT (P=0.005; Table 5).
Table 5.
IVT influence analysis. The influence of IVT on favorable outcomes, symptomatic ICH (SICH), or death (3M-mRS=6) with different treatment procedures.
| mTICI (2–3)/IVT+ | mTICI (2–3)/IVT− | OR (95% CI) | P | |
|---|---|---|---|---|
| Procedure | ||||
| ADAPT | 76/78 | 27/28 | 1.41 (0.12; 16.15) | 0.783 |
| SRFL | 114/130 | 56/63 | 0.89 (0.35; 2.29) | 0.810 |
| Solumbra | 42/50 | 15/15 | Insufficient number of observations | NA |
| MT + stent | 46/52 | 26/28 | 0.59 (0.11; 3.14) | 0.532 |
| CP | 34/42 | 17/17 | Insufficient number of observations | NA |
| 3M-mRS (0–2)/IVT+ | 3M-mRS (0–2)/IVT− | OR (95% CI) | P | |
| Procedure | ||||
| ADAPT | 35/69 | 9/25 | 1.83 (0.71; 4.70) | 0.185 |
| SRFL | 66/129 | 21/61 | 2.00 (1.06; 3.75) | 0.031 |
| Solumbra | 14/44 | 2/12 | 2.33 (0.45; 12.09) | 0.303 |
| MT + stent | 18/48 | 9/27 | 1.20 (0.45; 3.23) | 0.718 |
| CP | 12/40 | 3/15 | 1.71 (0.41; 7.20) | 0.458 |
| 3M-mRS (6)/IVT+ | 3M-mRS (6)/IVT− | OR (95% CI) | P | |
| Procedure | ||||
| ADAPT | 14/69 | 8/25 | 0.54 (0.19; 1.51) | 0.236 |
| SRFL | 21/129 | 21/61 | 0.37 (0.18; 0.75) | 0.005 |
| Solumbra | 11/44 | 2/12 | 1.67 (0.32; 8.80) | 0.544 |
| MT + stent | 8/48 | 6/27 | 0.70 (0.21; 2.28) | 0.553 |
| CP | 9/40 | 5/15 | 0.58 (0.16; 2.14) | 0.411 |
| SICH/IVT+ | SICH/IVT− | OR (95% CI) | P | |
| Procedure | ||||
| ADAPT | 12/78 | 2/28 | 2.36 (0.49; 11.30) | 0.269 |
| SRFL | 23/132 | 9/61 | 1.22 (0.53; 2.82) | 0.643 |
| Solumbra | 13/50 | 2/13 | 1.93 (0.38; 9.90) | 0.423 |
| MT + stent | 5/53 | 3/28 | 0.87 (0.19; 3.93) | 0.854 |
| CP | 11/41 | 7/17 | 0.52 (0.16; 1.72) | 0.282 |
Values are the number of patients with the indicated outcome/the total number in that group; OR – odds ratio; 95% CI – 95% confidence interval; P-values were evaluated with the chi-square test of independence.
Discussion
Recently, several studies have compared the contact aspiration ADAPT and SRFL techniques. The ASTER randomized clinical trial found no significant difference in successful revascularization rates at the end of the procedure (ADAPT: 85.4% versus SRFL: 83.1%; P=0.530) [24,25]. Almandoz et al. compared the Solumbra and ADAPT techniques for LVO recanalization in 100 patients, showing that patients in the ADAPT group achieved significantly higher rates of favorable 90-day clinical outcomes than patients in the Solumbra group (P=0.015). They also found that the use of the ADAPT technique (P=0.049) was an independent predictor of a favorable clinical outcome at 90 days in their cohort [26].
Primiani et al. performed a systematic PubMed search and statistical analysis to compare ADAPT and primary SRFL thrombectomy. They identified 38 publications and a total of 3028 patients who underwent thrombectomy with a stent retriever device and 29 publications and a total of 2413 patients who underwent a thrombectomy with ADAPT. They found no significant difference in successful recanalization rates (mTICI score=2b or 3) between the ADAPT (83.2%) and SRFL (75.9%) approaches (P=0.404). They also found no significant difference in the frequency of favorable clinical outcomes (3M-mRS=0–2) between the ADAPT (46.7%) and SRFL (46.5%) approaches (P=0.955) [27].
The choice between general anesthesia and conscious sedation is a controversial issue for mechanical thrombectomy procedures. Bekelis studied 1174 patients and found that, compared to conscious sedation, general anesthesia was associated with 6.4% increased fatality and 8.4 days longer stay in the hospital after mechanical thrombectomy. However, a comparative literature review by Illyas showed no significant differences in the favorable outcome rates (P=0.510) or successful reperfusion rates (P=0.390) between these 2 types of anesthesia. General anesthesia showed a significantly higher association with the development of pneumonia compared to conscious sedation (P=0.010) [28,29]. In our study, no significant difference was found in clinical outcomes with the different types of anesthesia used for LVO recanalization (Figure 1). The outcomes mostly depended on the times associated with patient transportation (mothership vs. drip-and-ship paradigm) or the procedure duration.
The latest types of neurointerventional devices were strongly associated with higher recanalization rates, better clinical outcomes, and shorter procedure times [30–33]. Our observations suggested that the ADAPT and SRFL procedures could be characterized by shorter procedure times compared to the Solumbra, MT + stent, or CP techniques (Figure 2).
The clinical outcome of the mechanical thrombectomy procedures also significantly differed according to the stroke location. The worst outcomes were found in posterior fossa procedures, despite the lack of significant differences among the different types of mechanical thrombectomy procedures used (Figure 3) [34].
Mechanical thrombectomies performed with a newer device for the ADAPT or SRFL techniques had higher rates of successful recanalization than mechanical thrombectomies performed with the older techniques like intra-arterial thrombolysis or with the first types of thrombectomy devices [35,36]. In our study, LVO recanalization of mTICI scores 2–3 were achieved in 98 (98%) patients with the ADAPT and 170 (87%) patients with the SRFL technique. Also, successful recanalization, with mTICI scores 2–3, were related to favorable clinical outcomes. Patients treated with ADAPT had significantly increased odds of achieving favorable mTICI scores and favorable clinical outcome (NIHSS after 7 days) compared to patients treated with the other techniques. Patients treated with SRFL had significantly increased odds of achieving a favorable long-term clinical status (3M-mRS=0–2; Table 4) compared to patients treated with the other techniques.
Despite great progress in recanalization techniques for treating brain LVOs, around 40–45% of procedures fail to achieve favorable clinical outcomes. This can be explained by failures to extract cardiac-origin emboli; IVT failure due to old organized thrombi with a large amount of Von Willebrand factor, neutrophils, fibrin, platelets, and free DNA (NETosis); and a resistance to fibrinolytic therapy and inflammatory brain reactions to the ischemia [37–40].
Prior IVT administration efficacy in the LVO has an important influence on the mechanical thrombectomy outcome. Lapergue et al. found significantly higher recanalization rates with the ADAPT than with the SRFL technique. However, they found an imbalance in prior rt-PA use; it was used more often in the ADAPT group (66.1%) than in the Solitaire group (45.4%). Nevertheless, the adjusted analysis for all confounding factors, including rt-PA use, confirmed a higher rate of recanalization in the ADAPT group [41].
Our analysis suggests that treatments with/without IVT only affected the SRFL procedure outcomes (Table 5) and the use of IVT had no effect on the outcomes of other treatment approaches. The direct effect of IVT use with adjunctive mechanical thrombectomy remains controversial. This controversy is linked to the uncertain roles played by IVT resistance to the “old-cardiac” emboli and the rate of periprocedural embolization in the new territory of the partially lysed and fragmented thrombi [42–44].
Prior IVT administration can increase the risk of symptomatic or non-symptomatic ICH [7,42,45,46]. We did not find any significant differences in the number of symptomatic ICH events between treatment groups treated with/without IVT prior to mechanical thrombectomy (Table 5).
The times between stroke onset and the diagnostic CT scan and between onset and the endovascular treatment in eligible patients with LVO are critical factors that influence the 3M-mRS clinical outcome. Recent research discussed the mothership and drip-and-ship paradigm and related time parameters [47–49]. The ESCAPE trial confirmed that every 30-min increase in the CT-to-reperfusion time significantly reduced the probability (by 8.3%) of achieving an outcome of functional independence (3M-mRS=0–2). Also, the onset-to-arrival (at the endovascular hospital) time was 42% (34 min) longer among patients who received intravenous alteplase at the referring hospital (drip-and-ship) compared to patients who underwent a direct transfer (to the mothership) [47]. In our study, patients treated with the SRFL procedure who received a mothership transfer had significantly increased odds of achieving a favorable clinical status (3M-mRS) than patients treated with SRFL who underwent a drip-and-ship transfer (Table 6).
Table 6.
Comparison of mothership and drip-and-ship paradigm. Comparison of favorable outcomes, symptomatic ICH (SICH), or death (3M-mRS=6) among patients treated at the mothership or the drip-and-ship paradigm for the different treatment procedures.
| mTICI (2–3)/Mothership | mTICI (2–3)/Drip-and-Ship | OR (95% CI) | P | |
|---|---|---|---|---|
| Procedure | ||||
| ADAPT | 72/74 | 25/25 | Insufficient number of observations | NA |
| SRFL | 96/104 | 73/87 | 2.3 (0.92; 5.78) | 0.070 |
| Solumbra | 39/46 | 16/17 | 0.35 (0.04; 3.06) | 0.323 |
| MT + stent | 40/44 | 31/35 | 1.29 (0.30; 5.57) | 0.732 |
| CP | 30/34 | 19/23 | 1.58 (0.35; 7.08) | 0.549 |
| 3M-mRS (0–2)/Mothership | 3M-mRS (0–2)/Drip-and-Ship | OR (95% CI) | P | |
| Procedure | ||||
| ADAPT | 32/69 | 12/23 | 0.79 (0.31; 2.04) | 0.630 |
| SRFL | 55/101 | 32/87 | 2.06 (1.14; 3.69) | 0.015 |
| Solumbra | 11/42 | 5/13 | 0.57 (0.15; 2.11) | 0.395 |
| MT + stent | 16/41 | 11/34 | 1.34 (0.52; 3.47) | 0.549 |
| CP | 10/33 | 5/20 | 1.30 (0.37; 4.58) | 0.678 |
| 3M-mRS (6)/Mothership | 3M-mRS (6)/Drip-and-Ship | OR (95% CI) | P | |
| Procedure | ||||
| ADAPT | 15/69 | 6/23 | 0.79 (0.26; 2.35) | 0.667 |
| SRFL | 18/101 | 22/87 | 0.64 (0.32; 1.29) | 0.212 |
| Solumbra | 9/42 | 4/13 | 0.61 (0.15; 2.46) | 0.488 |
| MT + stent | 11/41 | 3/34 | 3.79 (1.00; 14.94) | 0.046 |
| CP | 7/33 | 6/20 | 0.63 (0.18; 2.24) | 0.471 |
| SICH/Mothership | SICH/Drip-and-Ship | OR (95% CI) | P | |
| Procedure | ||||
| ADAPT | 9/74 | 5/25 | 0.55 (0.17; 1.84) | 0.331 |
| SRFL | 15/105 | 17/86 | 0.68 (0.32; 1.45) | 0.313 |
| Solumbra | 9/45 | 5/17 | 0.60 (0.17; 2.14) | 0.429 |
| MT + stent | 5/44 | 3/36 | 1.41 (0.31; 6.35) | 0.653 |
| CP | 8/33 | 8/23 | 0.6 (0.19; 1.93) | 0.390 |
Values are the number of patients with the indicated outcome/the total number in that group; OR – odds ratio; 95% CI – 95% confidence interval; P-values were evaluated with the chi-square test of independence.
The present study has certain limitations and defects. Firstly, the results are based on the collected data from the prospective observational study, which is at risk of confounding bias. A prospective randomized study could be more valid but also could violate ethical standards. Also, analyzing very specific groups of patients entails smaller sample sizes. Hence, it cannot be excluded that some significant differences were overlooked. Importantly, some specific groups were not represented at all, especially for the collateral scoring and CT perfusion analysis.
Conclusions
We showed that using the latest types of neurointerventional devices for ADAPT and SRFL procedures provided significant improvements in the properties of these procedures compared to the other examined single and combined techniques. These novel techniques (ADAPT and SRFL) provided shorter procedure times, higher recanalization rates, and more favorable clinical outcomes after treating an LVO with mechanical thrombectomy. A mothership transfer and IVT administration had direct effects on the SRFL approach for treating acute ischemic stroke. Our results suggest that the clinical outcome of mechanical thrombectomy procedures could be improved by further shortening the recanalization time, including a shorter drip-and-ship transfer time.
Abbreviations
- ADAPT
a direct aspiration first-pass technique
- A2-ACA
A2 segment of anterior cerebral artery
- CP
combined procedure
- CT
computed tomography
- DSA
digital subtraction angiography
- ICH
intracerebral hemorrhage
- IQR
interquartile range
- IVT
intravenous thrombolysis
- LVO
large-vessel occlusion
- M2-MCA
M2 segment of middle cerebral artery
- MT
mechanical thrombectomy
- mTICI
modified thrombolysis in cerebral infarction
- MRI
magnetic resonance imaging
- 3M-mRS
3-month modified Rankin Scale
- NIHSS
National Institutes of Health Stroke Scale
- P2-PCA
P2 segment of posterior cerebral artery
- SAH
subarachnoid hemorrhage
- SRFL
stent retriever first line
Footnotes
Source of support: This work was supported by the Ministry of Health, Institutional Grant – DRO-FNOs/2016 and by the VŠB-Technical University of Ostrava (project no. SP2018/68)
Conflicts of interest
None.
Ethics
The design of the study and informed consent were approved by the local ethics committees 639/2017.
References
- 1.Rentzos A, Lundqvist C, Karlsson JE, et al. Mechanical embolectomy for acute ischemic stroke in the anterior cerebral circulation: The Gothenburg experience during 2000–2011. Am J Neuroradiol. 2014;35:1936–41. doi: 10.3174/ajnr.A3997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Gobin YP, Starkman S, Duckwiler GR, et al. MERCI 1: A phase 1 study of mechanical embolus removal in cerebral ischemia. Stroke. 2004;35:2848–54. doi: 10.1161/01.STR.0000147718.12954.60. [DOI] [PubMed] [Google Scholar]
- 3.Smith WS, Sung G, Starkman S, et al. Safety and efficacy of mechanical embolectomy in acute ischemic stroke: Results of the MERCI trial. Stroke. 2005;36:1432–38. doi: 10.1161/01.STR.0000171066.25248.1d. [DOI] [PubMed] [Google Scholar]
- 4.Saver JL, Jahan R, Levy EI, et al. Solitaire flow restoration device versus the Merci Retriever in patients with acute ischaemic stroke (SWIFT): A randomised, parallel-group, non-inferiority trial. Lancet. 2012;380:1241–49. doi: 10.1016/S0140-6736(12)61384-1. [DOI] [PubMed] [Google Scholar]
- 5.Nogueira RG, Lutsep HL, Gupta R, et al. Trevo versus Merci retrievers for thrombectomy revascularisation of large vessel occlusions in acute ischaemic stroke (TREVO 2): A randomised trial. Lancet. 2012;380:1231–40. doi: 10.1016/S0140-6736(12)61299-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Kidwell CS, Jahan R, Gornbein J, et al. A trial of imaging selection and endovascular treatment for ischemic stroke. N Engl J Med. 2013;368:914–23. doi: 10.1056/NEJMoa1212793. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Broderick JP, Palesch YY, Demchuk AM, et al. Endovascular therapy after intravenous t-PA versus t-PA alone for stroke. N Engl J Med. 2013;368:893–903. doi: 10.1056/NEJMoa1214300. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Ciccone A, Valvassori L, Investigators SE. Endovascular treatment for acute ischemic stroke. N Engl J Med. 2013;368:2433–34. doi: 10.1056/NEJMc1304759. [DOI] [PubMed] [Google Scholar]
- 9.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: 10.1056/NEJMoa1411587. [DOI] [PubMed] [Google Scholar]
- 10.Goyal M, Demchuk AM, Menon BK, et al. Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med. 2015;372:1019–30. doi: 10.1056/NEJMoa1414905. [DOI] [PubMed] [Google Scholar]
- 11.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;10:439–48. doi: 10.1111/ijs.12459. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Campbell BC, Mitchell PJ, Kleinig TJ, et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med. 2015;372:1009–18. doi: 10.1056/NEJMoa1414792. [DOI] [PubMed] [Google Scholar]
- 13.Jovin TG, Chamorro A, Cobo E, et al. Thrombectomy within 8 hours after symptom onset in ischemic stroke. N Engl J Med. 2015;372:2296–306. doi: 10.1056/NEJMoa1503780. [DOI] [PubMed] [Google Scholar]
- 14.Wahlgren N, Moreira T, Michel P, et al. Mechanical thrombectomy in acute ischemic stroke: Consensus statement by ESO-Karolinska Stroke Update 2014/2015, supported by ESO, ESMINT, ESNR and EAN. Int J Stroke. 2016;11:134–47. doi: 10.1177/1747493015609778. [DOI] [PubMed] [Google Scholar]
- 15.Starck EE, McDermott JC, Crummy AB, et al. Percutaneous aspiration thromboembolectomy. Radiology. 1985;156:61–66. doi: 10.1148/radiology.156.1.3159042. [DOI] [PubMed] [Google Scholar]
- 16.Penumbra Pivotal Stroke Trial Investigators. The penumbra pivotal stroke trial: safety and effectiveness of a new generation of mechanical devices for clot removal in intracranial large vessel occlusive disease. Stroke. 2009;40:2761–68. doi: 10.1161/STROKEAHA.108.544957. [DOI] [PubMed] [Google Scholar]
- 17.Behme D, Kowoll A, Mpotsaris A, et al. Multicenter clinical experience in over 125 patients with the Penumbra Separator 3D for mechanical thrombectomy in acute ischemic stroke. J Neurointerv Surg. 2016;8:8–12. doi: 10.1136/neurintsurg-2014-011446. [DOI] [PubMed] [Google Scholar]
- 18.Kang DH, Hwang YH, Kim YS, et al. Direct thrombus retrieval using the reperfusion catheter of the penumbra system: Forced-suction thrombectomy in acute ischemic stroke. Am J Neuroradiol. 2011;32:283–87. doi: 10.3174/ajnr.A2299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Turk AS, Spiotta A, Frei D, et al. Initial clinical experience with the ADAPT technique: A direct aspiration first pass technique for stroke thrombectomy. J Neurointerv Surg. 2014;6:231–37. doi: 10.1136/neurintsurg-2013-010713. [DOI] [PubMed] [Google Scholar]
- 20.Kang DH, Park J. Endovascular stroke therapy focused on stent retriever thrombectomy and direct clot aspiration: Historical review and modern application. J Korean Neurosurg Soc. 2017;60:335–47. doi: 10.3340/jkns.2016.0809.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Hu YC, Stiefel MF. Force and aspiration analysis of the ADAPT technique in acute ischemic stroke treatment. J Neurointerv Surg. 2016;8:244–46. doi: 10.1136/neurintsurg-2014-011563. [DOI] [PubMed] [Google Scholar]
- 22.Humphries W, Hoit D, Doss VT, et al. Distal aspiration with retrievable stent assisted thrombectomy for the treatment of acute ischemic stroke. J Neurointerv Surg. 2015;7:90–94. doi: 10.1136/neurintsurg-2013-010986. [DOI] [PubMed] [Google Scholar]
- 23.Mocco J, Zaidat OO, von Kummer R, et al. Aspiration thrombectomy after intravenous alteplase versus intravenous alteplase alone. Stroke. 2016;47:2331–38. doi: 10.1161/STROKEAHA.116.013372. [DOI] [PubMed] [Google Scholar]
- 24.Gory B, Lapergue B, Blanc R, et al. Contact aspiration versus stent retriever in patients with acute ischemic stroke with M2 occlusion in the ASTER randomized trial (contact aspiration versus stent retriever for successful revascularization) Stroke. 2018;49:461–64. doi: 10.1161/STROKEAHA.117.019598. [DOI] [PubMed] [Google Scholar]
- 25.Lapergue B, Blanc R, Gory B, et al. Effect of endovascular contact aspiration vs. stent retriever on revascularization in patients with acute ischemic stroke and large vessel occlusion: The ASTER randomized clinical trial. JAMA. 2017;318:443–52. doi: 10.1001/jama.2017.9644. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Delgado Almandoz JE, Kayan Y, Young ML, et al. Comparison of clinical outcomes in patients with acute ischemic strokes treated with mechanical thrombectomy using either Solumbra or ADAPT techniques. J Neurointerv Surg. 2016;8:1123–28. doi: 10.1136/neurintsurg-2015-012122. [DOI] [PubMed] [Google Scholar]
- 27.Primiani C, Primiani C, et al. Direct aspiration (ADAPT) and primary stent retriever thrombectomy for acute ischemic stroke: A systematic review of radiographic and clinical outcomes in 5441 patients (P4.214) [Supplement (2018): P4.214. Web.] [Google Scholar]
- 28.Bekelis K, Missios S, MacKenzie TA, et al. Anesthesia technique and outcomes of mechanical thrombectomy in patients with acute ischemic stroke. Stroke. 2017;48:361–66. doi: 10.1161/STROKEAHA.116.015343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Ilyas A, Chen CJ, Ding D, et al. Endovascular mechanical thrombectomy for acute ischemic stroke under general anesthesia versus conscious sedation: A systematic review and meta-analysis. World Neurosurg. 2018;112:e355–67. doi: 10.1016/j.wneu.2018.01.049. [DOI] [PubMed] [Google Scholar]
- 30.Blanc R, Redjem H, Ciccio G, et al. Predictors of the aspiration component success of a direct aspiration first pass technique (ADAPT) for the endovascular treatment of stroke reperfusion strategy in anterior circulation acute stroke. Stroke. 2017;48:1588–93. doi: 10.1161/STROKEAHA.116.016149. [DOI] [PubMed] [Google Scholar]
- 31.Maekawa K, Shibata M, Nakajima H, et al. Erythrocyte-rich thrombus is associated with reduced number of maneuvers and procedure time in patients with acute ischemic stroke undergoing mechanical thrombectomy. Cerebrovasc Dis Extra. 2018;8:39–49. doi: 10.1159/000486042. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Prothmann S, Friedrich B, Boeckh-Behrens T, et al. Aspiration thrombectomy in clinical routine interventional stroke treatment: Is this the end of the stent retriever era? Clin Neuroradiol. 2018;28:217–24. doi: 10.1007/s00062-016-0555-7. [DOI] [PubMed] [Google Scholar]
- 33.Volny O, Krajina A, Belaskova S, et al. Mechanical thrombectomy performs similarly in real world practice: A 2016 nationwide study from the Czech Republic. J Neurointerv Surg. 2018;10(8):741–45. doi: 10.1136/neurintsurg-2017-013534. [DOI] [PubMed] [Google Scholar]
- 34.Dornak T, Kral M, Sedlackova Z, et al. Predictors for intracranial hemorrhage following intravenous thrombolysis in posterior circulation stroke. Transl Stroke Res. 2018;9(6):582–88. doi: 10.1007/s12975-018-0608-0. [DOI] [PubMed] [Google Scholar]
- 35.del Zoppo GJ, Higashida RT, Furlan AJ, et al. PROACT: A phase II randomized trial of recombinant pro-urokinase by direct arterial delivery in acute middle cerebral artery stroke. PROACT Investigators. Prolyse in Acute Cerebral Thromboembolism. Stroke. 1998;29:4–11. doi: 10.1161/01.str.29.1.4. [DOI] [PubMed] [Google Scholar]
- 36.Furlan A, Higashida R, Wechsler L, et al. Intra-arterial prourokinase for acute ischemic stroke. The PROACT II study: A randomized controlled trial. Prolyse in Acute Cerebral Thromboembolism. JAMA. 1999;282:2003–11. doi: 10.1001/jama.282.21.2003. [DOI] [PubMed] [Google Scholar]
- 37.Prochazka V, Jonszta T, Czerny D, et al. The role of von Willebrand factor, ADAMTS13, and cerebral artery thrombus composition in patient outcome following mechanical thrombectomy for acute ischemic stroke. Med Sci Monit. 2018;24:3929–45. doi: 10.12659/MSM.908441. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.De Meyer SF, Andersson T, Baxter B, et al. Analyses of thrombi in acute ischemic stroke: A consensus statement on current knowledge and future directions. Int J Stroke. 2017;12:606–14. doi: 10.1177/1747493017709671. [DOI] [PubMed] [Google Scholar]
- 39.De Candia E. NETosis in arterial and venous thrombosis: A one size fits all mechanism? Intern Emerg Med. 2017;12:9–11. doi: 10.1007/s11739-016-1600-x. [DOI] [PubMed] [Google Scholar]
- 40.Gragnano F, Sperlongano S, Golia E, et al. The role of von Willebrand factor in vascular inflammation: From pathogenesis to targeted therapy. Mediators Inflamm. 2017;2017 doi: 10.1155/2017/5620314. 5620314. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Lapergue B, Blanc R, Guedin P, et al. A direct aspiration, first pass technique (ADAPT) versus stent retrievers for acute stroke therapy: An observational comparative study. Am J Neuroradiol. 2016;37(10):1860–65. doi: 10.3174/ajnr.A4840. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Guedin P, Larcher A, Decroix JP, et al. Prior IV thrombolysis facilitates mechanical thrombectomy in acute ischemic stroke. J Stroke Cerebrovasc Dis. 2015;24:952–57. doi: 10.1016/j.jstrokecerebrovasdis.2014.12.015. [DOI] [PubMed] [Google Scholar]
- 43.Chueh JY, Puri AS, Wakhloo AK, Gounis MJ. Risk of distal embolization with stent retriever thrombectomy and ADAPT. J Neurointerv Surg. 2016;8:197–202. doi: 10.1136/neurintsurg-2014-011491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Morelli N, Rota E, Michieletti E, Guidetti D. Mechanical thrombectomy after intravenous thrombolysis for acute ischaemic stroke. Lancet Neurol. 2017;16:103–4. doi: 10.1016/S1474-4422(16)30379-9. [DOI] [PubMed] [Google Scholar]
- 45.Mistry EA, Mistry AM, Nakawah MO, et al. Mechanical thrombectomy outcomes with and without intravenous thrombolysis in stroke patients: A meta-analysis. Stroke. 2017;48:2450–56. doi: 10.1161/STROKEAHA.117.017320. [DOI] [PubMed] [Google Scholar]
- 46.Sanak D, Kocher M, Veverka T, et al. The safety and efficacy of bridging full-dose IV-IA thrombolysis in acute ischemic stroke patients with MCA occlusion: A comparison with IV thrombolysis alone. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2014;158:391–96. doi: 10.5507/bp.2013.003. [DOI] [PubMed] [Google Scholar]
- 47.Menon BK, Sajobi TT, Zhang Y, et al. Analysis of workflow and time to treatment on thrombectomy outcome in the endovascular treatment for small core and proximal occlusion ischemic stroke (ESCAPE) randomized, controlled trial. Circulation. 2016;133:2279–86. doi: 10.1161/CIRCULATIONAHA.115.019983. [DOI] [PubMed] [Google Scholar]
- 48.Deguchi I, Mizuno S, Kohyama S, et al. Drip-and-Ship thrombolytic therapy for acute ischemic stroke. J Stroke Cerebrovasc Dis. 2018;27:61–67. doi: 10.1016/j.jstrokecerebrovasdis.2017.07.033. [DOI] [PubMed] [Google Scholar]
- 49.Wang H, Thevathasan A, Dowling R, et al. Streamlining workflow for endovascular mechanical thrombectomy: Lessons learned from a comprehensive stroke center. J Stroke Cerebrovasc Dis. 2017;26:1655–62. doi: 10.1016/j.jstrokecerebrovasdis.2017.04.021. [DOI] [PubMed] [Google Scholar]