Abstract
Background
Increasing evidence of circadian biology may influence the physiopathologic mechanism, progression, and recovery of stroke. However, few data have shown about circadian rhythm on futile recanalization (FR) in patients treated with endovascular treatment (EVT).
Methods
From 2017 to 2021, an observational cohort of acute ischemic stroke (AIS) patients with large vessel occlusion (LVO) underwent EVT was conducted. FR was defined as the failure to achieve functional independence in patients at 90 days after EVT, although the occluded vessels reached a recanalization. The effect of circadian rhythm on FR was investigated using the logistic regression model.
Results
Of 783 patients, there were 149 patients who had stroke onset between 23:00-6:59, 318 patients between 7:00-14:59, and 316 patients between 15:00-22:59. Patients suffered from stroke during 15:00-22:59 had shorter OTP (p =0.001) time, shorter OTR (p<0.001) time, higher rate of intravenous thrombolysis (p =0.001) than groups of other time intervals. The rate of FR post-EVT in patients who had a stroke between 15:00-22:59 was significantly higher than in those with stroke onset between 23:00-6:59 (p =0.017). After adjusting for confounding factors, the time of stroke occurring during 15:00-22:59 (adjusted OR [aOR], 1.652; 95%CI, 1.024-2.666, p =0.04) was an independent predictor of FR.
Conclusion
Circadian rhythm can directly or indirectly affect the occurrence, development, and prognosis of AIS. More studies may be needed in the future to validate the results of our study and to explore the potential mechanisms behind the effects of circadian rhythms on FR.
Keywords: AIS, endovascular treatment, futile recanalization, circadian rhythm, outcome, LVO
1. INTRODUCTION
Acute Ischemic Stroke (AIS) due to large vessel occlusion (LVO) is associated with higher mortality and disability. The most effective treatment for LVO is rapid revascularization therapy. Patients with AIS who achieve recanalization post EVT and still have poor neurological function prognosis at 90 days are referred to as “futile recanalization (FR)” [1, 2]. The Reperfusion Efficacy Evaluation of multiple Stroke Endovascular Therapy Trials (HERMES) study suggested that one-third of patients achieved FR [3]. The results of RESCUE-RE showed that the proportion of FR is 49% in the real world in China [4].
So far, the mechanism of FR remains unclear, and exploring its predictive factors is of great value for early identification of poor prognosis after endovascular therapy. Previous studies have found a series of risk factors, mainly including old age, stroke severity, collateral circulation, and final infarct volume [2, 5, 6]. Increasing data have shown that clock genes and circadian rhythm have important effects on the occurrence, pathophysiological mechanism, progression, and recovery of AIS [7]. However, few studies have explored whether circadian rhythms also play a role in FR. Thus, the objective of our study was to assess the association between time of onset and the rate of FR in patients who underwent EVT.
2. METHODS
2.1. Study Design and Data Source
This study was conducted based on an observational cohort registered at Xuanwu Hospital, Capital Medical University. This prospective registry had been approved by the Ethics Committee. All patients or their legally authorized representatives were required to give both verbal and written consent upon admission. Consecutive AIS patients who underwent EVT were recruited in Xuanwu Hospital between January 2013 to June 2021. The inclusion criteria were 1) AIS secondary to LVO, 2) received modified treatment in cerebral ischemia (mTICI)≥2b/3a after recanalization treatment, and 3) available information of clinical data and function outcomes at 90 days.
2.2. Data Collection
The assessment data of patients included demographics, risk factors of cerebrovascular diseases, baseline National Institutes of Health Stroke Scale (NIHSS), Alberta Stroke Program Early CT Score (ASPECTS) or posterior circulation Alberta Stroke Program Early Computed Tomography Score (pc-ASPECTS), intravenous thrombolysis, time intervals, blood pressure, etiologies, symptomatic intracerebral hemorrhage (sICH), clinical functional outcomes at 3-month measured by modified Rankin Scale (mRS). Two experienced radiologists who were unaware of the clinical information of the patients evaluated the neuroimaging data independently. They were required to reach a consensus with regard to disagreement. Clinical outcomes were confirmed through standardized telephone interviews or clinical visits conducted by an investigator who was also unaware of the procedure. FR was defined as mRS > 2 scores at 90 days after successful vascular recanalization treatment (mTICI≥2b/3a). Patients were divided by binary time segmentations (23:00-06:59/ 07:00-22:59) and 8-h intervals (23:00-06:59/07:00-14:59/ 15:00-22:59) according to the recommendations of the Leducq Consortium International pour la Recherche Circadienne sur l’AVC Effects in Stroke (CIRCA) [8].
2.3. Statistical Analyses
All statistical analyses were conducted using IBM SPSS Statistics 27 (IBM Corp, Armonk, New York, USA), and significance was described as p < 0.05 (2-sided). According to the results of the normality test, continuous variables were displayed as mean±SD or median with interquartile range. Differences in continuous variables were confirmed using the Student t-test or Mann-Whitney U-test. Categorical variables were indicated as numbers (percentages). The chi-square test or Fisher exact test was applied for the comparisons between categorical data. The multivariable logistic regression was conducted to explore the role of the time of stroke onset in FR. The potential confounding factors (age, gender, hypertension, diabetes mellitus, hyperlipidemia, coronary heart disease, atrial fibrillation, ischemic stroke, intracranial hemorrhage, premorbid mRS, NIHSS, ASPECTS, treatment with IV alteplase, OTR time, SBP, DBP, posterior circulation infarct, sICH) were adjusted in this multivariable analysis based on the univariable logistic regression.
3. RESULTS
Of 906 AIS patients who received EVT, 850 patients achieved reperfusion after EVT, and 783 AIS patients eventually enrolled in this analysis. The flow chart of inclusion is demonstrated in Fig. (1).
Fig. (1).
Flow chart. Abbreviations: AIS=acute ischemic stroke, EVT=endovascular treatment, mTICI=modified treatment in cerebral ischemia.
While patients were categorized into groups based on the binary time segmentations, 634 patients had symptom onset in the daytime (7:00-22:59), and 149 patients had symptom onset in the nighttime (23:00-6:59). Patients during the daytime were likely to treat with IV alteplase (36.6% vs. 21.5%, p < 0.001), have shorter OTP time (370 vs. 450, p < 0.001), OTR time (443 vs. 513, p < 0.001) compared with patients during nighttime (23:00-6:59) (Table 1).
Table 1.
Baseline characteristics in binary time segmentations.
| Variables | 7:00-22:59 (n=634) | 23:00-6:59 (n=149) | p Value |
|---|---|---|---|
| Demographics | |||
| Age | 63 (56-72) | 64 (53-71) | 0.175 |
| Male | 182 (28.7) | 50 (33.6) | 0.243 |
| Medical History | |||
| Hypertension | 448 (70.7) | 101 (67.8) | 0.490 |
| Diabetes mellitus | 183 (28.9) | 42 (28.2) | 0.870 |
| Hyperlipidemia | 371 (58.5) | 81 (54.4) | 0.356 |
| Coronary heart disease | 136 (21.5) | 24 (16.1) | 0.145 |
| Atrial fibrillation | 216 (34.1) | 42 (28.2) | 0.169 |
| Ischemic stroke | 174 (27.4) | 39 (26.2) | 0.754 |
| Intracranial hemorrhage | 10 (1.6) | 1 (0.7) | 0.398 |
| Clinical Characteristics | |||
| Premorbid mRS | 0 (0-0) | 0 (0-0) | 0.261 |
| NIHSS | 16 (12-22) | 15 (11-21) | 0.165 |
| ASPECTS | 9 (7-10) | 9 (8-10) | 0.439 |
| Treatment with IV alteplase | 232 (36.6) | 32 (21.5) | <0.001 |
| Time Intervals | |||
| OTP time | 370 (279-505) | 450 (313-637) | <0.001 |
| OTR time | 443 (345.0-578.5) | 513 (390.5-724.5) | <0.001 |
| SBP | 146 (131-164) | 144 (130-160) | 0.264 |
| DBP | 83 (75-91) | 82 (76-90) | 0.716 |
| Posterior circulation infarct | 184 (29.0) | 40 (26.8) | 0.597 |
| TOAST | - | - | 0.049 |
| Large artery atherosclerosis | 366 (57.7) | 100 (67.1) | - |
| Cardioembolism | 242 (38.2) | 41 (27.5) | - |
| Other or undetermined | 26 (4.1) | 8 (5.4) | - |
| sICH | 76 (12.0) | 13 (8.7) | 0.259 |
Abbreviations: NIHSS=National Institutes of Health Stroke Scale, ASPECTS=Alberta Stroke Program Early CT Score, IV= intravenous injection, OTP= time from onset to puncture, OTR=time from onset to reperfusion, SBP=systolic blood pressure, DBP= diastolic blood pressure, TOAST=etiology according to the Trial of Org 10172 in Acute Stroke Treatment, sICH= symptomatic intracerebral hemorrhage.
Based on the 8-h intervals, 149 patients had symptom onset during 23:00-6:59, 318 patients had symptom onset during 7:00-14:59, and 316 patients had symptom onset during 15:00-22:59. Patients with stroke onset during 15:00-22:59 were more likely to treat with IV alteplase when compared to other periods throughout the day (p =0.001). Compared with other time intervals, patients with short OTP (p =0.001) and OTR (p < 0.001) time tended to suffer from stroke during 15:00-22:59 (Table 2).
Table 2.
Baseline characteristics in segmentations of 8-h intervals.
| Variables | 23:00-6:59 (n=149) | 7:00-14:59 (n=318) | 15:00-22:59 (n=316) | p Value |
|---|---|---|---|---|
| Demographics | ||||
| Age | 64 (53-71) | 64 (55-72) | 63 (56-71) | 0.151 |
| Male | 50 (33.6) | 92 (28.9) | 90 (28.5) | 0.502 |
| Medical History | ||||
| Hypertension | 101 (67.8) | 217 (68.2) | 231 (73.1) | 0.322 |
| Diabetes mellitus | 42 (28.2) | 90 (28.3) | 93 (29.4) | 0.939 |
| Hyperlipidemia | 81 (54.4) | 176 (55.3) | 195 (61.7) | 0.175 |
| Coronary heart disease | 24 (16.1) | 66 (20.8) | 70 (22.2) | 0.315 |
| Atrial fibrillation | 42 (28.2) | 104 (32.7) | 112 (35.4) | 0.297 |
| Ischemic stroke | 39 (26.2) | 85 (26.7) | 89 (28.2) | 0.877 |
| Intracranial hemorrhage | 1 (0.7) | 3 (0.9) | 7 (2.2) | 0.277 |
| Clinical Characteristics | ||||
| Premorbid mRS | 0 (0-0) | 0 (0-0) | 0 (0-0) | 0.474 |
| NIHSS | 15 (11-21) | 16 (12-21) | 17 (12-22) | 0.337 |
| ASPECTS | 9 (8-10) | 9 (7-10) | 9 (7-10) | 0.467 |
| Treatment with IV alteplase | 32 (21.5) | 109 (34.3) | 123 (38.9) | 0.001 |
| Time Intervals | ||||
| OTP time | 450 (313-637) | 380 (284.5-506.5) | 362 (267.5-500.5) | 0.001 |
| OTR time | 513 (390.5-724.5) | 450 (343.5-570) | 438.5 (345-586) | <0.001 |
| SBP | 144 (130-160) | 147 (130-163) | 146 (133-166) | 0.418 |
| DBP | 82 (76-90) | 83 (75-90) | 83 (75-92) | 0.862 |
| Posterior circulation infarct | 40 (26.8) | 95 (29.9) | 89 (28.2) | 0.776 |
| TOAST | - | - | - | 0.140 |
| Large artery atherosclerosis | 100 (67.1) | 179 (56.3) | 187 (59.2) | - |
| Cardioembolism | 41 (27.5) | 124 (39.0) | 118 (37.3) | - |
| Other or undetermined | 8 (5.4) | 15 (4.7) | 11 (3.5) | - |
| sICH | 13 (8.7) | 38 (11.9) | 38 (12.0) | 0.528 |
Abbreviations: NIHSS=National Institutes of Health Stroke Scale, ASPECTS=Alberta Stroke Program Early CT Score, IV= intravenous injection, OTP= time from onset to puncture, OTR=time from onset to reperfusion, SBP=systolic blood pressure, DBP= diastolic blood pressure, TOAST=etiology according to the Trial of Org 10172 in Acute Stroke Treatment, sICH= symptomatic intracerebral hemorrhage.
The rate of FR after EVT in patients with stroke onset during 23:00-6:59 was 49.66%, and 61.20% during 7:00-22:59 based on binary time segmentations. In terms of the segmentations of 8-h intervals, the rate of FR was 58.49% during 7:00-14:59, 63.92% during 15:00-22:59, and 49.66% during 23:00-6:59. (Fig. 2) The patients with stroke onset in the 23:00-6:59 time were more likely to experience FR than those in 7:00-22:59 (p =0.01). FR was significantly associated with groups between the 15:00-22:59 time and 23:00-6:59 (p =0.017). In the violin plot, the distribution of onset time for patients with FR does not show a significant difference compared to that of patients without FR. However, the time-specificity of FR occurring between 0:00-5:00 time is slightly more obvious than that of effective reperfusion (Fig. 3).
Fig. (2).
Clinical outcome after successful reperfusion at 3 months. (a) Distribution of modified Rankin Scale scores at 3 months post EVT in binary segmentations. (b) Distribution of modified Rankin Scale scores at 3 months post EVT in each 8-h interval.
Fig. (3).
The rate of futile recanalization in different time segmentations. (a) Comparison between groups of binary segmentations. (b) Comparison between groups of 8-h intervals. (c) Time of onset between patients with and without FR. Abbreviation: FR= futile recanalization.
In the multivariable analysis, no significant difference was found between binary segmentations of time of stroke onset and FR after adjusting for other covariates in model 1. In the model, the time of stroke occurring during 15:00-22:59 (adjusted OR [aOR], 1.652; 95%CI [Confidence Interval], 1.024-2.666, p =0.04) was identified as an independent factor for predicting FR. And age (aOR, 1.668; 95%CI, 1.092-2.546, p =0.018), male (aOR, 1.039; 95%CI, 1.021-1.058, p < 0.001), hypertension (aOR, 0.661; 95%CI, 0.440-0.994, p =0.047), diabetes mellitus (aOR, 1.570; 95%CI, 1.052-2.343, p =0.027), hyperlipidemia (aOR, 2.818; 95%CI, 1.980-4.011, p < 0.001), NIHSS (aOR, 1.096; 95%CI, 1.069-1.122, p < 0.001), ASPECTS (aOR, 0.880; 95%CI, 0.785-0.986, p =0.027), DBP (aOR, 1.019; 95%CI, 1.002-1.035, p =0.025) were also related to FR (Table 3).
Table 3.
Multivariate analysis of between circadian rhythm and futile recanalization.
| Model 1 | Model 2 | ||||
|---|---|---|---|---|---|
| Variables | Adjusted OR (95% CI) | p Value | Variables | Adjusted OR (95% CI) | p Value |
| Age | 1.656 (1.085-2.527) | 0.019 | Age | 1.668 (1.092-2.546) | 0.018 |
| Male | 1.039 (1.021-1.058) | < 0.001 | Male | 1.039 (1.021-1.058) | < 0.001 |
| Hypertension | 0.669 (0.445-1.005) | 0.053 | Hypertension | 0.661 (0.440-0.994) | 0.047 |
| Diabetes mellitus | 1.573 (1.055-2.347) | 0.026 | Diabetes mellitus | 1.570 (1.052-2.343) | 0.027 |
| Hyperlipidemia | 2.831 (1.990-4.027) | < 0.001 | Hyperlipidemia | 2.818 (1.980-4.011) | < 0.001 |
| Coronary heart disease | 1.299 (0.813-2.074) | 0.274 | Coronary heart disease | 1.306 (0.817-2.086) | 0.265 |
| Atrial fibrillation | 0.950 (0.604-1.493) | 0.823 | Atrial fibrillation | 0.936 (0.594-1.474) | 0.775 |
| Ischemic stroke | 1.419 (0.915-2.200) | 0.118 | Ischemic stroke | 1.422 (0.915-2.208) | 0.117 |
| Premorbid mRS | 0.956 (0.688-1.327) | 0.787 | Premorbid mRS | 0.957 (0.689-1.329) | 0.791 |
| NIHSS | 1.096 (1.070-1.123) | < 0.001 | NIHSS | 1.096 (1.069-1.122) | < 0.001 |
| ASPECTS | 0.880 (0.785-0.986) | 0.028 | ASPECTS | 0.880 (0.785-0.986) | 0.027 |
| Posterior circulation infarct | 0.938 (0.598-1.471) | 0.779 | Posterior circulation infarct | 0.946 (0.802-1.485) | 0.809 |
| SBP | 1.006 (0.996-1.016) | 0.223 | SBP | 1.006 (0.996-1.016) | 0.223 |
| DBP | 1.019 (1.002-1.035) | 0.026 | DBP | 1.019 (1.002-1.035) | 0.025 |
| sICH | 11.101 (4.592-26.837) | < 0.001 | sICH | 11.048 (4.570-26.705) | < 0.001 |
| Binary segmentations | - | - | 8-h intervals | - | - |
| 7:00-22:59 | Reference | - | 23:00-6:59 | Reference | 0.118 |
| 23:00-6:59 | 0.670 (0.433-1.037) | 0.072 | 7:00-14:59 | 1.353 (0.843-2.173) | 0.210 |
| - | - | - | 15:00-22:59 | 1.652 (1.024-2.666) | 0.040 |
Abbreviations: NIHSS=National Institutes of Health Stroke Scale, ASPECTS=Alberta Stroke Program Early CT Score, SBP=systolic blood pressure, DBP= diastolic blood pressure, TOAST=etiology according to the Trial of Org 10172 in Acute Stroke Treatment, sICH= symptomatic intracerebral hemorrhage.
4. DISCUSSION
In our study, we found that patients with stroke onset between 15:00-22:59 were more likely to achieve FR than those with stroke onset between 23:00-6:59. And in the multivariate logistic regression analysis, the time of stroke onset between 15:00-22:59 was the independent influence factor of FR after EVT.
Although FR is an important phenomenon that affects outcomes of patients, and its pathogenesis is not well understood. The status of collateral circulation and microvascular injury are relatively clear mechanisms affecting the FR [9]. Previous studies have shown that the common influencing factors for FR include old age, NIHSS at baseline, ASPECTS at baseline, anterior or posterior circulation, time of thrombectomy, and so on. The circadian rhythm is an intrinsic physiological cycle inherent to all living organisms that spans approximately 24 hours and regulates internal physiological functions in response to environmental changes. In mammals, circadian rhythms are governed by the biological clock [10]. While previous research observed the association between time of day and the clinical outcomes of AIS, it remains uncertain what the role of circadian rhythm is in FR. Most previous studies have shown that patients who had stroke onset at nighttime were more prone to have a poor prognosis. Wang et al. reported that patients with stroke occurring 00:00-06:00 and 06:00-12:00 tended to achieve favorable outcomes [11]. Burbano et al. suggested that morning treatment (05:00-10:59) was related to the lowest mRS scores at 90 days and successful recanalization [12]. A multicenter observational cohort study from Korea revealed that night-onset (18:00-22:00 and 22:00-02:00) stroke was more likely to achieve early neurological deterioration (END) and had a lower likelihood of favorable outcomes [13]. Similarly, another study found that patients disfavored EVT start times at 15:55-17:15 and 18:55-20:55 on working [14]. However, the time intervals of these studies are not uniform. In order to make the time division more standardized and rationalized, our research is in accordance with the latest consensus recommendations of the Leducq network on Circadian Effects in Stroke [8]. Consistent with most previous studies, we have further confirmed patients with stroke onset at the end of the day (15:00-22:59) benefit less from thrombectomy.
The occurrence of stroke follows a circadian rhythm, mainly related to the fluctuations of sympathetic nerve activity, blood pressure, coagulation factors, platelet aggregation, etc., and the circadian rhythms of these factors are controlled by endogenous clocks [15-17]. The potential mechanism of these results may be as follows. Firstly, previous experimental data in rats showed that the ischemic penumbra during the active phase in AIS was narrower than that during the resting period [18]. Accordingly, the active period of the human is the time of the day, which indicates that the cerebral infarction tissue saved by reperfusion during the day is less than that at night when AIS occurs. Secondly, preclinical data showed that the cerebral intravascular blood flow regulation had a circadian rhythm [7, 18]. Previous studies have shown that impaired automatic regulation of cerebral blood flow and venous outflow have been confirmed as possible mechanisms of FR [19, 20]. Therefore, using Transcranial Doppler (TCD) for continuous monitoring of cerebral autoregulation and CTA for venous outflow in the future will facilitate further investigation into the underlying mechanism through which circadian rhythm impacts reperfusion efficacy. Thirdly, circadian biology may impact the pathophysiology of BBB and edema following reperfusion, which may further lead to FR [7]. Additionally, body temperature between 15:00-22:59, the higher level of the day, perhaps results in a poor prognosis for patients after EVT, even if the vessel is successfully recanalization [21].
Some limitations should be considered. Firstly, our study was a single-center design, which may bring about the presence of selection bias. Secondly, imaging data were not included in our multivariate analysis because of the limited storage time of information about neuroimaging. Thirdly, some new indicators related to stroke circadian rhythm, such as vascular reactivity, are expected to be prospective studies in the future because relevant data have not been collected.
CONCLUSION
There is accumulating evidence indicating that circadian rhythms influence stroke onset, pathophysiology, outcomes, and recovery in patients with AIS. Our study found the circadian rhythm that was associated with FR, and further research is warranted to explore the management of AIS patients who underwent EVT according to the circadian rhythm.
LIST OF ABBREVIATIONS
- AIS
Acute Ischemic Stroke
- ASPECTS
Alberta Stroke Program Early CT Score
- END
Early Neurological Deterioration
- FR
Futile Recanalization
- LVO
Large Vessel Occlusion
- NIHSS
National Institutes of Health Stroke Scale
- TCD
Transcranial Doppler
AUTHORS’ CONTRIBUTIONS
Mengke Zhang analyzed the data and drafted the manuscript. Xian Wang, Xi Chen, Jiali Xu, Wenting Guo, Changhong Ren, Sijie Li, and Wenbo Zhao collected the data. Chuanjie Wu revised the manuscript. Xunming Ji and Chuanjie Wu contributed to supervision and administration.
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
This study was approved by the Institutional Ethics Committee of Xuanwu Hospital of Capital Medical University [Approval No. (2017) 030].
HUMAN AND ANIMAL RIGHTS
All procedures conducted in studies involving human participants adhered to the ethical standards set forth by institutional and/or research committees, as well as the 1975 Declaration of Helsinki, with its 2013 revision.
CONSENT FOR PUBLICATION
All patients or their legally authorized representatives were required to give both verbal and written consent upon admission.
STANDARDS OF REPORTING
STROBE guidelines were followed.
AVAILABILITY OF DATA AND MATERIALS
The data and supportive information are available upon request from the corresponding author.
FUNDING
This work was financially supported by [National Natural Science Foundation of China] (Grant number: 82027802) and [National Key Research and Development Program] (Grant number: 2022YFC3602401).
CONFLICT OF INTEREST
The authors declare no conflict of interest, financial or otherwise.
ACKNOWLEDGEMENTS
Declared none.
REFERENCES
- 1.Albers G.W., Marks M.P., Kemp S., Christensen S., Tsai J.P., Ortega-Gutierrez S., McTaggart R.A., Torbey M.T., Kim-Tenser M., Leslie-Mazwi T., Sarraj A., Kasner S.E., Ansari S.A., Yeatts S.D., Hamilton S., Mlynash M., Heit J.J., Zaharchuk G., Kim S., Carrozzella J., Palesch Y.Y., Demchuk A.M., Bammer R., Lavori P.W., Broderick J.P., Lansberg M.G. Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N. Engl. J. Med. 2018;378(8):708–718. doi: 10.1056/NEJMoa1713973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.van Horn N., Kniep H., Leischner H., McDonough R., Deb-Chatterji M., Broocks G., Thomalla G., Brekenfeld C., Fiehler J., Hanning U., Flottmann F. Predictors of poor clinical outcome despite complete reperfusion in acute ischemic stroke patients. J. Neurointerv. Surg. 2021;13(1):14–18. doi: 10.1136/neurintsurg-2020-015889. [DOI] [PubMed] [Google Scholar]
- 3.Goyal M., Menon B.K., van Zwam W.H., Dippel D.W.J., Mitchell P.J., Demchuk A.M., Dávalos A., Majoie C.B.L.M., van der Lugt A., de Miquel M.A., Donnan G.A., Roos Y.B.W.E.M., Bonafe A., Jahan R., Diener H.C., van den Berg L.A., Levy E.I., Berkhemer O.A., Pereira V.M., Rempel J., Millán M., Davis S.M., Roy D., Thornton J., Román L.S., Ribó M., Beumer D., Stouch B., Brown S., Campbell B.C.V., van Oostenbrugge R.J., Saver J.L., Hill M.D., Jovin T.G. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):1723–1731. doi: 10.1016/S0140-6736(16)00163-X. [DOI] [PubMed] [Google Scholar]
- 4.Liu D., Nie X., Pan Y., Yan H., Pu Y., Wei Y., Cai Y., Ding Y., Lu Q., Zhang Z., Gu W., Hou X., Yang Z., Wen M., Wang P., Ma G., Ma N., Miao Z., Leng X., Yan B., Davis S.M., Wang Y., Liu L. Adverse outcomes associated with higher mean blood pressure and greater blood pressure variability immediately after successful embolectomy in those with acute ischemic stroke, and the influence of pretreatment collateral circulation status. J. Am. Heart Assoc. 2021;10(5):e019350. doi: 10.1161/JAHA.120.019350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Groot A.E., Treurniet K.M., Jansen I.G.H., Lingsma H.F., Hinsenveld W., van de Graaf R.A., Roozenbeek B., Willems H.C., Schonewille W.J., Marquering H.A., van den Berg R., Dippel D.W.J., Majoie C.B.L.M., Roos Y.B.W.E.M., Coutinho J.M., Dippel D.W.J., Lugt A., Majoie C.B.L.M., Roos Y.B.W.E.M., van Oostenbrugge R.J., van Zwam W.H., Boiten J., Vos J.A., Jansen I.G.H., Mulder M.J.H.L., Goldhoorn R.J.B., Schonewille W.J., Coutinho J.M., Wermer M.J.H., van Walderveen M.A.A., Staals J., Hofmeijer J., Martens J.M., Lycklama à Nijeholt G.J., Roozenbeek B., Emmer B.J., de Bruijn S.F., van Dijk L.C., van der Worp H.B., Lo R.H., van Dijk E.J., Boogaarts H.D., de Kort P.L.M., Peluso J.J.P., van den Berg J.S.P., van Hasselt B.A.A.M., Aerden L.A.M., Dallinga R.J., Uyttenboogaart M., Eshghi O., Schreuder T.H.C.M.L., Heijboer R.J.J., Keizer K., Yo L.S.F., den Hertog H.M., Sturm E.J.C., Sprengers M.E.S., Jenniskens S.F.M., den Berg R., Yoo A.J., Beenen L.F.M., Postma A.A., Roosendaal S.D., van der Kallen B.F.W., van den Wijngaard I.R., van Es A.C.G.M., Bot J., Jan van Doormaal P., Flach H.Z., Lingsma H.F., Ghannouti N., Sterrenberg M., Puppels C., Pellikaan W., Sprengers R., Elfrink M., de Meris J., Vermeulen T., Geerlings A., van Vemde G., Simons T., van Rijswijk C., Messchendorp G., Bongenaar H., Bodde K., Kleijn S., Lodico J., Droste H., Wollaert M., Jeurrissen D., Bos E., Drabbe Y., Zweedijk B., Khalilzada M., Venema E., Chalos V., Compagne K.C.J., Geuskens R.R., Straaten T., Ergezen S., Harmsma R.R.M., Muijres D., de Jong A., Hinsenveld W., Berkhemer O.A., Boers A.M.M., Huguet J., Groot P.F.C., Mens M.A., van Kranendonk K.R., Kappelhof M., Tolhuijsen M.L., Alves H. Endovascular treatment in older adults with acute ischemic stroke in the MR CLEAN Registry. Neurology. 2020;95(2):e131–e139. doi: 10.1212/WNL.0000000000009764. [DOI] [PubMed] [Google Scholar]
- 6.Campbell B.C.V., Majoie C.B.L.M., Albers G.W., Menon B.K., Yassi N., Sharma G., van Zwam W.H., van Oostenbrugge R.J., Demchuk A.M., Guillemin F., White P., Dávalos A., van der Lugt A., Butcher K.S., Cherifi A., Marquering H.A., Cloud G., Macho Fernández J.M., Madigan J., Oppenheim C., Donnan G.A., Roos Y.B.W.E.M., Shankar J., Lingsma H., Bonafé A., Raoult H., Hernández-Pérez M., Bharatha A., Jahan R., Jansen O., Richard S., Levy E.I., Berkhemer O.A., Soudant M., Aja L., Davis S.M., Krings T., Tisserand M., San Román L., Tomasello A., Beumer D., Brown S., Liebeskind D.S., Bracard S., Muir K.W., Dippel D.W.J., Goyal M., Saver J.L., Jovin T.G., Hill M.D., Mitchell P.J., Berkhemer O.A., Fransen P.S.S., Beumer D., van den Berg L.A., Lingsma H.F., Yoo A.J., Schonewille W.J., Vos J.A., Nederkoorn P.J., Wermer M.J.H., van Walderveen M.A.A., Staals J., Hofmeijer J., van Oostayen J.A., Lycklama à Nijeholt G.J., Boiten J., Brouwer P.A., Emmer B.J., de Bruijn S.F., van Dijk L.C., Kappelle J., Lo R.H., van Dijk E.J., de Vries J., de Kort P.L.M., van Rooij W.J.J., van den Berg J.S.P., van Hasselt B.A.A.M., Aerden L.A.M., Dallinga R.J., Visser M.C., Bot J.C.J., Vroomen P.C., Eshghi O., Schreuder T.H.C.M.L., Heijboer R.J.J., Keizer K., Tielbeek A.V., den Hertog H.M., Gerrits D.G., van den Berg-Vos R.M., Karas G.B., Steyerberg E.W., Flach Z., Marquering H.A., Sprengers M.E.S., Jenniskens S.F.M., Beenen L.F.M., van den Berg R., Koudstaal P.J., van Zwam W.H., Roos Y.B.W.E.M., van der Lugt A., van Oostenbrugge R.J., Majoie C.B.L.M., Dippel D.W.J., Brown M.M., Liebig T., Stijnen T., Andersson T., Mattle H., Wahlgren N., van der Heijden E., Ghannouti N., Fleitour N., Hooijenga I., Puppels C., Pellikaan W., Geerling A., Lindl-Velema A., van Vemde G., de Ridder A., Greebe P., de Bont-Stikkelbroeck J., de Meris J., Janssen K., Struijk W., Licher S., Boodt N., Ros A., Venema E., Slokkers I., Ganpat R-J., Mulder M., Saiedie N., Heshmatollah A., Schipperen S., Vinken S., van Boxtel T., Koets J., Boers M., Santos E., Borst J., Jansen I., Kappelhof M., Lucas M., Geuskens R., Barros R.S., Dobbe R., Csizmadia M., Hill M.D., Goyal M., Demchuk A.M., Menon B.K., Eesa M., Ryckborst K.J., Wright M.R., Kamal N.R., Andersen L., Randhawa P.A., Stewart T., Patil S., Minhas P., Almekhlafi M., Mishra S., Clement F., Sajobi T., Shuaib A., Montanera W.J., Roy D., Silver F.L., Jovin T.G., Frei D.F., Sapkota B., Rempel J.L., Thornton J., Williams D., Tampieri D., Poppe A.Y., Dowlatshahi D., Wong J.H., Mitha A.P., Subramaniam S., Hull G., Lowerison M.W., Sajobi T., Salluzzi M., Wright M.R., Maxwell M., Lacusta S., Drupals E., Armitage K., Barber P.A., Smith E.E., Morrish W.F., Coutts S.B., Derdeyn C., Demaerschalk B., Yavagal D., Martin R., Brant R., Yu Y., Willinsky R.A., Montanera W.J., Weill A., Kenney C., Aram H., Stewart T., Stys P.K., Watson T.W., Klein G., Pearson D., Couillard P., Trivedi A., Singh D., Klourfeld E., Imoukhuede O., Nikneshan D., Blayney S., Reddy R., Choi P., Horton M., Musuka T., Dubuc V., Field T.S., Desai J., Adatia S., Alseraya A., Nambiar V., van Dijk R., Wong J.H., Mitha A.P., Morrish W.F., Eesa M., Newcommon N.J., Shuaib A., Schwindt B., Butcher K.S., Jeerakathil T., Buck B., Khan K., Naik S.S., Emery D.J., Owen R.J., Kotylak T.B., Ashforth R.A., Yeo T.A., McNally D., Siddiqui M., Saqqur M., Hussain D., Kalashyan H., Manosalva A., Kate M., Gioia L., Hasan S., Mohammad A., Muratoglu M., Williams D., Thornton J., Cullen A., Brennan P., O’Hare A., Looby S., Hyland D., Duff S., McCusker M., Hallinan B., Lee S., McCormack J., Moore A., O’Connor M., Donegan C., Brewer L., Martin A., Murphy S., O’Rourke K., Smyth S., Kelly P., Lynch T., Daly T., O’Brien P., O’Driscoll A., Martin M., Daly T., Collins R., Coughlan T., McCabe D., Murphy S., O’Neill D., Mulroy M., Lynch O., Walsh T., O’Donnell M., Galvin T., Harbison J., McElwaine P., Mulpeter K., McLoughlin C., Reardon M., Harkin E., Dolan E., Watts M., Cunningham N., Fallon C., Gallagher S., Cotter P., Crowe M., Doyle R., Noone I., Lapierre M., Coté V.A., Lanthier S., Odier C., Durocher A., Raymond J., Weill A., Daneault N., Deschaintre Y., Jankowitz B., Baxendell L., Massaro L., Jackson-Graves C., Decesare S., Porter P., Armbruster K., Adams A., Billigan J., Oakley J., Ducruet A., Jadhav A., Giurgiutiu D-V., Aghaebrahim A., Reddy V., Hammer M., Starr M., Totoraitis V., Wechsler L., Streib S., Rangaraju S., Campbell D., Rocha M., Gulati D., Silver F.L., Krings T., Kalman L., Cayley A., Williams J., Stewart T., Wiegner R., Casaubon L.K., Jaigobin C., del Campo J.M., Elamin E., Schaafsma J.D., Willinsky R.A., Agid R., Farb R., ter Brugge K., Sapkoda B.L., Baxter B.W., Barton K., Knox A., Porter A., Sirelkhatim A., Devlin T., Dellinger C., Pitiyanuvath N., Patterson J., Nichols J., Quarfordt S., Calvert J., Hawk H., Fanale C., Frei D.F., Bitner A., Novak A., Huddle D., Bellon R., Loy D., Wagner J., Chang I., Lampe E., Spencer B., Pratt R., Bartt R., Shine S., Dooley G., Nguyen T., Whaley M., McCarthy K., Teitelbaum J., Tampieri D., Poon W., Campbell N., Cortes M., Dowlatshahi D., Lum C., Shamloul R., Robert S., Stotts G., Shamy M., Steffenhagen N., Blacquiere D., Hogan M., AlHazzaa M., Basir G., Lesiuk H., Iancu D., Santos M., Choe H., Weisman D.C., Jonczak K., Blue-Schaller A., Shah Q., MacKenzie L., Klein B., Kulandaivel K., Kozak O., Gzesh D.J., Harris L.J., Khoury J.S., Mandzia J., Pelz D., Crann S., Fleming L., Hesser K., Beauchamp B., Amato-Marzialli B., Boulton M., Lopez- Ojeda P., Sharma M., Lownie S., Chan R., Swartz R., Howard P., Golob D., Gladstone D., Boyle K., Boulos M., Hopyan J., Yang V., Da Costa L., Holmstedt C.A., Turk A.S., Navarro R., Jauch E., Ozark S., Turner R., Phillips S., Shankar J., Jarrett J., Gubitz G., Maloney W., Vandorpe R., Schmidt M., Heidenreich J., Hunter G., Kelly M., Whelan R., Peeling L., Burns P.A., Hunter A., Wiggam I., Kerr E., Watt M., Fulton A., Gordon P., Rennie I., Flynn P., Smyth G., O’Leary S., Gentile N., Linares G., McNelis P., Erkmen K., Katz P., Azizi A., Weaver M., Jungreis C., Faro S., Shah P., Reimer H., Kalugdan V., Saposnik G., Bharatha A., Li Y., Kostyrko P., Santos M., Marotta T., Montanera W., Sarma D., Selchen D., Spears J., Heo J.H., Jeong K., Kim D.J., Kim B.M., Kim Y.D., Song D., Lee K-J., Yoo J., Bang O.Y., Rho S., Lee J., Jeon P., Kim K.H., Cha J., Kim S.J., Ryoo S., Lee M.J., Sohn S-I., Kim C-H., Ryu H-G., Hong J-H., Chang H-W., Lee C-Y., Rha J., Davis S.M., Donnan G.A., Campbell B.C.V., Mitchell P.J., Churilov L., Yan B., Dowling R., Yassi N., Oxley T.J., Wu T.Y., Silver G., McDonald A., McCoy R., Kleinig T.J., Scroop R., Dewey H.M., Simpson M., Brooks M., Coulton B., Krause M., Harrington T.J., Steinfort B., Faulder K., Priglinger M., Day S., Phan T., Chong W., Holt M., Chandra R.V., Ma H., Young D., Wong K., Wijeratne T., Tu H., Mackay E., Celestino S., Bladin C.F., Loh P.S., Gilligan A., Ross Z., Coote S., Frost T., Parsons M.W., Miteff F., Levi C.R., Ang T., Spratt N., Kaauwai L., Badve M., Rice H., de Villiers L., Barber P.A., McGuinness B., Hope A., Moriarty M., Bennett P., Wong A., Coulthard A., Lee A., Jannes J., Field D., Sharma G., Salinas S., Cowley E., Snow B., Kolbe J., Stark R., King J., Macdonnell R., Attia J., D’Este C., Saver J.L., Goyal M., Diener H-C., Levy E.I., Bonafé A., Mendes Pereira V., Jahan R., Albers G.W., Cognard C., Cohen D.J., Hacke W., Jansen O., Jovin T.G., Mattle H.P., Nogueira R.G., Siddiqui A.H., Yavagal D.R., von Kummer R., Smith W., Turjman F., Hamilton S., Chiacchierini R., Amar A., Sanossian N., Loh Y., Devlin T., Baxter B., Hawk H., Sapkota B., Quarfordt S., Sirelkhatim A., Dellinger C., Barton K., Reddy V.K., Ducruet A., Jadhav A., Horev A., Giurgiutiu D-V., Totoraitis V., Hammer M., Jankowitz B., Wechsler L., Rocha M., Gulati D., Campbell D., Star M., Baxendell L., Oakley J., Siddiqui A., Hopkins L.N., Snyder K., Sawyer R., Hall S., Costalat V., Riquelme C., Machi P., Omer E., Arquizan C., Mourand I., Charif M., Ayrignac X., Menjot de Champfleur N., Leboucq N., Gascou G., Moynier M., du Mesnil de Rochemont R., Singer O., Berkefeld J., Foerch C., Lorenz M., Pfeilschifer W., Hattingen E., Wagner M., You S.J., Lescher S., Braun H., Dehkharghani S., Belagaje S.R., Anderson A., Lima A., Obideen M., Haussen D., Dharia R., Frankel M., Patel V., Owada K., Saad A., Amerson L., Horn C., Doppelheuer S., Schindler K., Lopes D.K., Chen M., Moftakhar R., Anton C., Smreczak M., Carpenter J.S., Boo S., Rai A., Roberts T., Tarabishy A., Gutmann L., Brooks C., Brick J., Domico J., Reimann G., Hinrichs K., Becker M., Heiss E., Selle C., Witteler A., Al-Boutros S., Danch M-J., Ranft A., Rohde S., Burg K., Weimar C., Zegarac V., Hartmann C., Schlamann M., Göricke S., Ringlestein A., Wanke I., Mönninghoff C., Dietzold M., Budzik R., Davis T., Eubank G., Hicks W.J., Pema P., Vora N., Mejilla J., Taylor M., Clark W., Rontal A., Fields J., Peterson B., Nesbit G., Lutsep H., Bozorgchami H., Priest R., Ologuntoye O., Barnwell S., Dogan A., Herrick K., Takahasi C., Beadell N., Brown B., Jamieson S., Hussain M.S., Russman A., Hui F., Wisco D., Uchino K., Khawaja Z., Katzan I., Toth G., Cheng-Ching E., Bain M., Man S., Farrag A., George P., John S., Shankar L., Drofa A., Dahlgren R., Bauer A., Itreat A., Taqui A., Cerejo R., Richmond A., Ringleb P., Bendszus M., Möhlenbruch M., Reiff T., Amiri H., Purrucker J., Herweh C., Pham M., Menn O., Ludwig I., Acosta I., Villar C., Morgan W., Sombutmai C., Hellinger F., Allen E., Bellew M., Gandhi R., Bonwit E., Aly J., Ecker R.D., Seder D., Morris J., Skaletsky M., Belden J., Baker C., Connolly L.S., Papanagiotou P., Roth C., Kastrup A., Politi M., Brunner F., Alexandrou M., Merdivan H., Ramsey C., Given C., II, Renfrow S., Deshmukh V., Sasadeusz K., Vincent F., Thiesing J.T., Putnam J., Bhatt A., Kansara A., Caceves D., Lowenkopf T., Yanase L., Zurasky J., Dancer S., Freeman B., Scheibe-Mirek T., Robison J., Rontal A., Roll J., Clark D., Rodriguez M., Fitzsimmons B-F.M., Zaidat O., Lynch J.R., Lazzaro M., Larson T., Padmore L., Das E., Farrow-Schmidt A., Hassan A., Tekle W., Cate C., Jansen O., Cnyrim C., Wodarg F., Wiese C., Binder A., Riedel C., Rohr A., Lang N., Laufs H., Krieter S., Remonda L., Diepers M., Añon J., Nedeltchev K., Kahles T., Biethahn S., Lindner M., Chang V., Gächter C., Esperon C., Guglielmetti M., Arenillas Lara J.F., Martínez Galdámez M., Calleja Sanz A.I., Cortijo Garcia E., Garcia Bermejo P., Perez S., Mulero Carrillo P., Crespo Vallejo E., Ruiz Piñero M., Lopez Mesonero L., Reyes Muñoz F.J., Brekenfeld C., Buhk J-H., Krützelmann A., Thomalla G., Cheng B., Beck C., Hoppe J., Goebell E., Holst B., Grzyska U., Wortmann G., Starkman S., Duckwiler G., Jahan R., Rao N., Sheth S., Ng K., Noorian A., Szeder V., Nour M., McManus M., Huang J., Tarpley J., Tateshima S., Gonzalez N., Ali L., Liebeskind D., Hinman J., Calderon-Arnulphi M., Liang C., Guzy J., Koch S., DeSousa K., Gordon-Perue G., Haussen D., Elhammady M., Peterson E., Pandey V., Dharmadhikari S., Khandelwal P., Malik A., Pafford R., Gonzalez P., Ramdas K., Andersen G., Damgaard D., Von Weitzel-Mudersbach P., Simonsen C., Ruiz de Morales Ayudarte N., Poulsen M., Sørensen L., Karabegovich S., Hjørringgaard M., Hjort N., Harbo T., Sørensen K., Deshaies E., Padalino D., Swarnkar A., Latorre J.G., Elnour E., El-Zammar Z., Villwock M., Farid H., Balgude A., Cross L., Hansen K., Holtmannspötter M., Kondziella D., Hoejgaard J., Taudorf S., Soendergaard H., Wagner A., Cronquist M., Stavngaard T., Cortsen M., Krarup L.H., Hyldal T., Haring H-P., Guggenberger S., Hamberger M., Trenkler J., Sonnberger M., Nussbaumer K., Dominger C., Bach E., Jagadeesan B.D., Taylor R., Kim J., Shea K., Tummala R., Zacharatos H., Sandhu D., Ezzeddine M., Grande A., Hildebrandt D., Miller K., Scherber J., Hendrickson A., Jumaa M., Zaidi S., Hendrickson T., Snyder V., Killer-Oberpfalzer M., Mutzenbach J., Weymayr F., Broussalis E., Stadler K., Jedlitschka A., Malek A., Mueller-Kronast N., Beck P., Martin C., Summers D., Day J., Bettinger I., Holloway W., Olds K., Arkin S., Akhtar N., Boutwell C., Crandall S., Schwartzman M., Weinstein C., Brion B., Prothmann S., Kleine J., Kreiser K., Boeckh-Behrens T., Poppert H., Wunderlich S., Koch M.L., Biberacher V., Huberle A., Gora-Stahlberg G., Knier B., Meindl T., Utpadel-Fischler D., Zech M., Kowarik M., Seifert C., Schwaiger B., Puri A., Hou S., Wakhloo A., Moonis M., Henninger N., Goddeau R., Massari F., Minaeian A., Lozano J.D., Ramzan M., Stout C., Patel A., Tunguturi A., Onteddu S., Carandang R., Howk M., Ribó M., Sanjuan E., Rubiera M., Pagola J., Flores A., Muchada M., Meler P., Huerga E., Gelabert S., Coscojuela P., Tomasello A., Rodriguez D., Santamarina E., Maisterra O., Boned S., Seró L., Rovira A., Molina C.A., Millán M., Muñoz L., Pérez de la Ossa N., Gomis M., Dorado L., López-Cancio E., Palomeras E., Munuera J., García Bermejo P., Remollo S., Castaño C., García-Sort R., Cuadras P., Puyalto P., Hernández-Pérez M., Jiménez M., Martínez-Piñeiro A., Lucente G., Dávalos A., Chamorro A., Urra X., Obach V., Cervera A., Amaro S., Llull L., Codas J., Balasa M., Navarro J., Ariño H., Aceituno A., Rudilosso S., Renu A., Macho J.M., San Roman L., Blasco J., López A., Macías N., Cardona P., Quesada H., Rubio F., Cano L., Lara B., de Miquel M.A., Aja L., Serena J., Cobo E., Albers G.W., Lees K.R., Arenillas J., Roberts R., Minhas P., Al-Ajlan F., Salluzzi M., Zimmel L., Patel S., Eesa M., Martí-Fàbregas J., Jankowitz B., Serena J., Salvat-Plana M., López-Cancio E., Bracard S., Ducrocq X., Anxionnat R., Baillot P-A., Barbier C., Derelle A-L., Lacour J-C., Richard S., Samson Y., Sourour N., Baronnet-Chauvet F., Clarencon F., Crozier S., Deltour S., Di Maria F., Le Bouc R., Leger A., Mutlu G., Rosso C., Szatmary Z., Yger M., Zavanone C., Bakchine S., Pierot L., Caucheteux N., Estrade L., Kadziolka K., Leautaud A., Renkes C., Serre I., Desal H., Guillon B., Boutoleau-Bretonniere C., Daumas-Duport B., De Gaalon S., Derkinderen P., Evain S., Herisson F., Laplaud D-A., Lebouvier T., Lintia-Gaultier A., Pouclet-Courtemanche H., Rouaud T., Rouaud Jaffrenou V., Schunck A., Sevin-Allouet M., Toulgoat F., Wiertlewski S., Gauvrit J-Y., Ronziere T., Cahagne V., Ferre J-C., Pinel J-F., Raoult H., Mas J-L., Meder J-F., Al Najjar-Carpentier A-A., Birchenall J., Bodiguel E., Calvet D., Domigo V., Godon-Hardy S., Guiraud V., Lamy C., Majhadi L., Morin L., Naggara O., Trystram D., Turc G., Berge J., Sibon I., Menegon P., Barreau X., Rouanet F., Debruxelles S., Kazadi A., Renou P., Fleury O., Pasco-Papon A., Dubas F., Caroff J., Godard Ducceschi S., Hamon M-A., Lecluse A., Marc G., Giroud M., Ricolfi F., Bejot Y., Chavent A., Gentil A., Kazemi A., Osseby G-V., Voguet C., Mahagne M-H., Sedat J., Chau Y., Suissa L., Lachaud S., Houdart E., Stapf C., Buffon Porcher F., Chabriat H., Guedin P., Herve D., Jouvent E., Mawet J., Saint-Maurice J-P., Schneble H-M., Turjman F., Nighoghossian N., Berhoune N-N., Bouhour F., Cho T-H., Derex L., Felix S., Gervais-Bernard H., Gory B., Manera L., Mechtouff L., Ritzenthaler T., Riva R., Salaris Silvio F., Tilikete C., Blanc R., Obadia M., Bartolini M.B., Gueguen A., Piotin M., Pistocchi S., Redjem H., Drouineau J., Neau J-P., Godeneche G., Lamy M., Marsac E., Velasco S., Clavelou P., Chabert E., Bourgois N., Cornut-Chauvinc C., Ferrier A., Gabrillargues J., Jean B., Marques A-R., Vitello N., Detante O., Barbieux M., Boubagra K., Favre Wiki I., Garambois K., Tahon F., Ashok V., Voguet C., Coskun O., Guedin P., Rodesch G., Lapergue B., Bourdain F., Evrard S., Graveleau P., Decroix J.P., Wang A., Sellal F., Ahle G., Carelli G., Dugay M-H., Gaultier C., Lebedinsky A.P., Lita L., Musacchio R.M., Renglewicz-Destuynder C., Tournade A., Vuillemet F., Montoro F.M., Mounayer C., Faugeras F., Gimenez L., Labach C., Lautrette G., Denier C., Saliou G., Chassin O., Dussaule C., Melki E., Ozanne A., Puccinelli F., Sachet M., Sarov M., Bonneville J-F., Moulin T., Biondi A., De Bustos Medeiros E., Vuillier F., Courtheoux P., Viader F., Apoil-Brissard M., Bataille M., Bonnet A-L., Cogez J., Kazemi A., Touze E., Leclerc X., Leys D., Aggour M., Aguettaz P., Bodenant M., Cordonnier C., Deplanque D., Girot M., Henon H., Kalsoum E., Lucas C., Pruvo J-P., Zuniga P., Bonafé A., Arquizan C., Costalat V., Machi P., Mourand I., Riquelme C., Bounolleau P., Arteaga C., Faivre A., Bintner M., Tournebize P., Charlin C., Darcel F., Gauthier-Lasalarie P., Jeremenko M., Mouton S., Zerlauth J-B., Lamy C., Hervé D., Hassan H., Gaston A., Barral F-G., Garnier P., Beaujeux R., Wolff V., Herbreteau D., Debiais S., Murray A., Ford G., Muir K.W., White P., Clifton A., Freeman J., Ford I., Markus H., Wardlaw J., Lees K.R., Molyneux A., Robinson T., Lewis S., Norrie J., Robertson F., Perry R., Dixit A., Cloud G., Clifton A., Madigan J., Roffe C., Nayak S., Lobotesis K., Smith C., Herwadkar A., Kandasamy N., Goddard T., Bamford J., Subramanian G., Lenthall R., Littleton E., Lamin S., Storey K., Ghatala R., Banaras A., Aeron-Thomas J., Hazel B., Maguire H., Veraque E., Harrison L., Keshvara R., Cunningham J. Penumbral imaging and functional outcome in patients with anterior circulation ischaemic stroke treated with endovascular thrombectomy versus medical therapy: a meta-analysis of individual patient-level data. Lancet Neurol. 2019;18(1):46–55. doi: 10.1016/S1474-4422(18)30314-4. [DOI] [PubMed] [Google Scholar]
- 7.Lo E.H., Albers G.W., Dichgans M., Donnan G., Esposito E., Foster R., Howells D.W., Huang Y.G., Ji X., Klerman E.B., Lee S., Li W., Liebeskind D.S., Lizasoain I., Mandeville E.T., Moro M.A., Ning M., Ray D., Sakadžić S., Saver J.L., Scheer F.A.J.L., Selim M., Tiedt S., Zhang F., Buchan A.M. Circadian biology and stroke. Stroke. 2021;52(6):2180–2190. doi: 10.1161/STROKEAHA.120.031742. [DOI] [PubMed] [Google Scholar]
- 8.Saver J.L., Klerman E.B., Buchan A.M., Calleja P., Lizasoain I., Bahr-Hosseini M., Lee S., Liebeskind D.S., Mergenthaler P., Mun K.T., Ning M., Pelz D., Ray D., Rothwell P.M., Seners P., Sreekrishnan A., Sung E.M., Tiedt S., Webb A.J.S., Wölfer T.A., Albers G.W. Consensus recommendations for standardized data elements, scales, and time segmentations in studies of human circadian/diurnal biology and stroke. Stroke. 2023;54(7):1943–1949. doi: 10.1161/STROKEAHA.122.041394. [DOI] [PubMed] [Google Scholar]
- 9.Kan Y., Li S., Zhang B., Ding Y., Zhao W., Ji X. No-reflow phenomenon following stroke recanalization therapy: Clinical assessment advances: A narrative review. Brain Circ. 2023;9(4):214–221. doi: 10.4103/bc.bc_37_23. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Zisapel N. New perspectives on the role of melatonin in human sleep, circadian rhythms and their regulation. Br. J. Pharmacol. 2018;175(16):3190–3199. doi: 10.1111/bph.14116. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Wang X., Wang X., Ma J., Jia M., Wu L., Li W., Li C., Wu C., Ren C., Chen X., Zhao W., Ji X. Association between the time of day at stroke onset and functional outcome of acute ischemic stroke patients treated with endovascular therapy. J. Cereb. Blood Flow Metab. 2022;42(12):2191–2200. doi: 10.1177/0271678X221111852. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Burbano V.G., Wölfer T.A., Vlegels N., Quandt F., Zimmermann H., Wischmann J., Kellert L., Liebig T., Dimitriadis K., Saver J.L., Tiedt S. Association of the time of day of EVT with clinical outcomes and benefit from successful recanalization after stroke. Ann. Clin. Transl. Neurol. 2023;10(10):1917–1923. doi: 10.1002/acn3.51877. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Ryu W.S., Hong K.S., Jeong S.W., Park J.E., Kim B.J., Kim J.T., Lee K.B., Park T.H., Park S.S., Park J.M., Kang K., Cho Y.J., Park H.K., Lee B.C., Yu K.H., Oh M.S., Lee S.J., Kim J.G., Cha J.K., Kim D.H., Lee J., Han M.K., Park M.S., Choi K.H., Lee J., Saver J.L., Lo E.H., Bae H.J., Kim D.E. Association of ischemic stroke onset time with presenting severity, acute progression, and long-term outcome: A cohort study. PLoS Med. 2022;19(2):e1003910. doi: 10.1371/journal.pmed.1003910. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Hajdu S.D., Kaesmacher J., Michel P., Sirimarco G., Knebel J.F., Bartolini B., Kurmann C.C., Puccinelli F., Mosimann P.J., Bonvin C., Arnold M., Niederhäuser J., Eskandari A., Mordasini P., Gralla J., Fischer U., Saliou G. Association of time of day when endovascular therapy for stroke starts and functional outcome. Neurology. 2021;96(8):e1124–e1136. doi: 10.1212/WNL.0000000000011449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Westgate E.J., Cheng Y., Reilly D.F., Price T.S., Walisser J.A., Bradfield C.A., FitzGerald G.A. Genetic components of the circadian clock regulate thrombogenesis in vivo. Circulation. 2008;117(16):2087–2095. doi: 10.1161/CIRCULATIONAHA.107.739227. [DOI] [PubMed] [Google Scholar]
- 16.Anea C.B., Zhang M., Stepp D.W., Simkins G.B., Reed G., Fulton D.J., Rudic R.D. Vascular disease in mice with a dysfunctional circadian clock. Circulation. 2009;119(11):1510–1517. doi: 10.1161/CIRCULATIONAHA.108.827477. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Rudic RD., Fulton DJ. Pressed for time: The circadian clock and hypertension. J. appl. physiol. 2009;107(4):1328–1338. doi: 10.1152/japplphysiol.00661.2009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Esposito E., Li W., T Mandeville E., Park J.H., Şencan I., Guo S., Shi J., Lan J., Lee J., Hayakawa K., Sakadžić S., Ji X., Lo E.H. Potential circadian effects on translational failure for neuroprotection. Nature. 2020;582(7812):395–398. doi: 10.1038/s41586-020-2348-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Nie X., Pu Y., Zhang Z., Liu X., Duan W., Liu L. Futile recanalization after endovascular therapy in acute ischemic stroke. BioMed Res. Int. 2018;2018:1–5. doi: 10.1155/2018/5879548. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Heitkamp C., Winkelmeier L., Heit J.J., Albers G.W., Lansberg M.G., Wintermark M., Broocks G., van Horn N., Kniep H.C., Sporns P.B., Zeleňák K., Fiehler J., Faizy T.D. Unfavorable cerebral venous outflow is associated with futile recanalization in acute ischemic stroke patients. Eur. J. Neurol. 2023;30(9):2684–2692. doi: 10.1111/ene.15898. [DOI] [PubMed] [Google Scholar]
- 21.Kräuchi K., Wirz-Justice A. Circadian rhythm of heat production, heart rate, and skin and core temperature under unmasking conditions in men. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1994;267(3):R819–R829. doi: 10.1152/ajpregu.1994.267.3.R819. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data and supportive information are available upon request from the corresponding author.