Abstract
Background
The comparison of mechanical thrombectomy (MT) outcomes between patients with the hyperdense middle cerebral artery sign (HMCAS) and non-HMCAS is important to evaluate the impact of this radiological finding on treatment efficacy. This meta-analysis aimed to assess the association between HMCAS and clinical outcomes in patients undergoing thrombectomy, comparing the outcomes over non-HMCAS.
Methods
A systematic literature search was conducted in PubMed, Ovid Embase, Google Scholar, and Cochrane Library to identify studies on MT outcomes for M1 occlusions of HMCAS over non-HMCAS. Inclusion criteria encompassed modified Rankin Scale (mRS) score, mortality, symptomatic intracranial hemorrhage (sICH), and successful recanalization. Using R software version 4.1.2, we calculated pooled odds ratios (ORs) and their corresponding 95% confidence intervals (CI).
Results
The meta-analysis was performed for 5 studies with 724 patients. There was no association found between presence of HMCAS and achieving mRS 0–2 (OR = 0.65, 95% CI: 0.29–1.47; p = .544). Mortality analysis also showed no significant association with presence of HMCAS (OR = 0.78, 95% CI: 0.37–1.65; p = .520). No significant difference in sICH risk (OR = 1.54, 95% CI: 0.24–9.66; p = .646) was found between groups. Recanalization analysis showed a non-significant positive association (OR = 1.23, 95% CI: 0.67–2.28; p = .501). Heterogeneity was observed in all analyses.
Conclusion
Our findings showed that there is no statistically significant difference in mRS scores, mortality, sICH, and recanalization success rates between the HMCAS and non-HMCAS groups.
Keywords: Hyperdense, middle cerebral artery, mechanical thrombectomy, stroke
Introduction
The identification of a hyperdense middle cerebral artery sign (HMCAS) on pretreatment CT scans is a common occurrence in patients with acute middle cerebral artery (MCA) occlusion. Its prevalence in such cases ranges from 17% to 50%,1,2 and it has been associated with more severe strokes upon presentation, 3 larger infarct volumes, 4 and unfavorable clinical outcomes. Prior research has suggested that intravenous thrombolysis is less effective in patients with HMCAS compared to those without it, which has led to the consideration of primary mechanical thrombectomy (MT) as an alternative treatment approached. 5
Recent advancements in MT techniques, utilizing stent retrievers or large-bore aspiration catheters, have shown promising results in achieving successful reperfusion rates of over 80% for emergent large vessel occlusion (ELVO) in the anterior and posterior circulation.6,7 Consequently, it is crucial to reassess the clinical implications of the hyperdense artery sign on pretreatment CT scans in this new era of MT for acute stroke management.8–11 Nevertheless, there is a scarcity of data regarding the prognostic value of the HMCAS in predicting outcomes after modern MT in patients with ELVO. Therefore, this study aims to investigate the potential relationship between the presence or absence of HMCAS on pretreatment CT and treatment outcomes following MT in patients with acute stroke due to MCA occlusions.
Methods
The systematic review followed the guidelines outlined in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statements. 12 The AutoLit platform (Nested Knowledge, St. Paul, Minnesota, USA) was utilized for conducting the search, 13 eliminating duplicate citations, and screening full texts.
Search strategy and selection criteria
Search strategies were created using a combination of keywords and standardized index terms. A literature search was conducted on PubMed, Web of Science, Ovid Medline, Ovid Embase, and Scopus using a combination of the terms (“Hyperdense” OR “Hyperdense MCA” OR “Middle Cerebral Artery” OR “MCA” OR “non hyperdense” OR “Non hyperdense MCA” AND (“thrombectomy” OR “mechanical thrombectomy” OR “stroke” OR “occlusion” OR, “endovascular,” “embolectomy,” “large-vessel,” “ischemic stroke,” “aspiration”). Moreover, we did an extensive manual search through the articles’ references to retrieve any missed papers.
Eligibility criteria and study selection
The inclusion criteria were hyperdense or non-hyperdense MCA treatment with MT, data availability on MT treatment complications and outcomes, and use of modern stent retriever or suction catheter, English language. No limitation to publication year was applied, and all publications up to May 20, 2023, were screened.
Exclusion criteria included literature reviews, systematic reviews, meta-analyses, case reports, case series consisting of <5 cases, abstracts, conference papers, anatomical or radiological studies, technical notes, non-English studies, and treated hyperdense or non-hyperdense MCA occlusions without MT.
Articles that do not provide separate outcomes for MCA occlusions with or without HMCAS were also excluded. The authors completed the initial title and abstract screening independently. Duplicates and overlapping data (studies published on the same registry) were omitted. Next, two investigators independently performed the full-text screening (YCS and AO). In case of conflict, the senior author (RK with more than 10 years of experience) resolved the disagreement.
Data extraction and study outcomes
Two reviewers (SA and YCS) independently screened articles. Duplicate articles were removed by matching the author, year, and title. Reviewers preliminarily screened the articles based on the inclusion criteria, and the final eligible studies were evaluated by reviewing the full texts. A manual search for additional relevant studies using references from retrieved articles was also performed. Conflicts were discussed with a third reviewer (RK) and resolved by mutual consensus.
The study focused on several key outcomes to evaluate the effectiveness of MT in patients with acute stroke due to MCA occlusions. These outcomes included successful recanalization, mortality, symptomatic intracranial hemorrhage (sICH), and functional independence. Recanalization, which refers to the restoration of blood flow, was assessed using the modified Treatment in Cerebral Infarctions (mTICI) scale. 14 A recanalization score of mTICI ≥2b was considered indicative of successful recanalization. Symptomatic intracranial hemorrhage (sICH) is a severe complication that can occur following the procedure. It was specifically evaluated in this study. Functional independence, measured by the modified Rankin Scale (mRS) score, was defined as a score of ≤2 at 90 days after the intervention. This outcome represents the patient’s ability to perform daily activities without assistance and is a significant measure of treatment success.
Quality assessment
The Newcastle–Ottawa Scale was used to assess the quality of all studies. 15 The Newcastle–Ottawa Scale contains eight items within three domains (selection, comparability, and outcome), with a maximum total score of 9. Studies with scores of 7–9 were classified as having a low risk, those with scores of 4–6 as moderate to high risk, and those with <4 as having a very high risk of bias. A senior author (RK) resolved any discrepancies among the reviewers by consensus.
Statistical analysis
The meta-analysis was conducted using R software version 4.3.0. Pooled prevalence rates and their corresponding 95% confidence intervals (CI) were computed. Given the presence of methodological heterogeneity among the included studies, a random effects model was employed to amalgamate the data. Moreover, we used the generalized linear mixed models (GLMMs) method for better stability with small studies and rare events.16,17 Heterogeneity was assessed utilizing Q statistics and the I2 test, with statistical significance set at I2 > 50% or a p-value <.05. In view of the limited number of studies within the compared subgroups (less than 10), examinations of publication bias (Egger’s regression test) and the impact of sample size (meta-regression) were not conducted. 18
Results
Search results and risk of bias assessment
Our initial search returned 661 results. After removing duplicates (149), a total of 512 studies were evaluated for screening. As a result of this initial screening, 506 entries were excluded. The remaining five articles were read in full text, and systematic review was prepared with the five studies (Online Supplementary Figure 1). Our risk of bias assessment identified four studies as being low risk of bias and one study as being at moderate risk of bias (Online Supplementary Table 1).
Baseline characteristics of studies
Table 1 summarizes the characteristics of the five included comparative studies (HMCAS vs non-HMCAS). All studies provided successful recanalization and functional independence data, but only four studies provided sICH and mortality data. A meta-analysis was also performed on the baseline characteristics of five studies with 724 patients (Online Supplementary Figures 2–4). Our analysis demonstrated that the HMCAS group had a significantly lower diabetes rate compared to the non-HMCAS group (OR: 0.46, 95% CI: 0.32 to 0.68, p < .001), and there was no heterogeneity among included studies (I2 = 0%, p = .921). Additionally, no significant differences were observed in terms of age, female sex, hypertension, hyperlipidemia, atrial fibrillation, previous TIA/stroke, smoker, and adjunctive IVT between HMCAS and non-HMCAS groups (p > .05); however, there were moderate heterogeneities in hypertension (I2 = 71%, p = .017), atrial fibrillation (I2 = 53%, p = .076), and previous TIA/stroke (I2 = 72%, p = .059).
Table 1.
Baseline characteristics of included studies.
| Authors | Total patient number | Age, years (mean±SD) | Female, n (%) | Diabetes, n (%) | Hypertension, n (%) | Hyperlipidemia, n (%) | Atrial fibrillation, n (%) | Previous TIA/stroke, n (%) | Smoker, n (%) | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| HMCAS | Non-HMCAS | HMCAS | Non-HMCAS | HMCAS | Non-HMCAS | HMCAS | Non-HMCAS | HMCAS | Non-HMCAS | HMCAS | Non-HMCAS | HMCAS | Non-HMCAS | HMCAS | Non-HMCAS | HMCAS | Non-HMCAS | |
| Man et. al., 2014 | 75 | 51 | 68.3±14.6 | 69.0±14.0 | 43 (57.0%) | 23 (45.0%) | 20 (26.6%) | 20 (39.2%) | 51 (68.0%) | 42 (82.3%) | 36 (48.0%) | 26 (50.9%) | 40 (53.3%) | 21 (41.1%) | N/A | N/A | 34 (45.3%) | 27 (52.9%) |
| Kim et. al., 2017 | 118 | 94 | 72.5±3.8 | 71.2±4.3 | 57 (48.7%) | 48 (51.1%) | 16 (13.5%) | 22 (23.4%) | 72 (61.0%) | 46 (48.9%) | 26 (22.0%) | 23 (24.4%) | 77 (65.2%) | 43 (45.7%) | 26 (22.0%) | 14 (14.8%) | 31 (26.2%) | 23 (24.4%) |
| Mowla et. al., 2021 | 46 | 47 | 67.8±12.2 | 67.7±14.7 | 20 (43.5%) | 26 (55.3%) | 5 (10.8%) | 13 (27.6%) | N/A | N/A | N/A | N/A | 19 (41.3%) | 20 (42.5%) | N/A | N/A | N/A | N/A |
| Ume et. al., 2022 | 71 | 31 | 67.9±16.1 | 71.5±15.4 | 41 (57.8%) | 22 (70.0%) | 14 (19.7%) | 11 (35.4%) | 54 (76.0%) | 29 (93.5%) | 40 (56.3%) | 19 (61.2%) | 21 (29.5%) | 13 (41.9%) | N/A | N/A | N/A | N/A |
| Merlino et. al., 2023 | 140 | 51 | 73.2±11.2 | 73.1±10.4 | 73 (52.1%) | 25 (49.0%) | 12 (8.5%) | 10 (19.6%) | 94 (67.1%) | 32 (62.7%) | 30 (21.4%) | 17 (33.3%) | 43 (30.7%) | 16 (31.3%) | 10 (7.1%) | 7 (1.4%) | 18 (12.8%) | 8 (15.6%) |
HMCAS: hyperdense middle cerebral artery sign, TIA: transient ischemic attack, N/A: not available, SD: standard deviation.
Favorable outcomes (mRS 0–2)
The random effects model analysis performed across five studies revealed a similar rate on achieving an mRS score of 0–2 in patients with an HMCAS compared to non-HMCAS (OR: 1.19, 95% CI: 0.67 to 2.11, p = .544); however, there was a moderate heterogeneity among included studies (I2 = 66%, p = .018) (Figure 1).
Figure 1.
Forest plot of mRS 0–2.
Mortality
For the mortality outcomes, pooled analysis conducted by four studies with 631 patients showed that there was no significant difference in mortality rates between the two groups (OR: 0.78, 95% CI: 0.37 to 1.65; p = .520). However, the heterogeneity analysis yielded moderate heterogeneity among the studies (I2 = 65%, p = .038) (Figure 2).
Figure 2.
Forest plot of mortality.
Symptomatic intracranial hemorrhage
Four studies with 622 patients were included to assess the risk of symptomatic intracranial hemorrhage (sICH) in patients with HMCAS compared to non-HMCAS. The results demonstrated that there was no significant difference in the risk of sICH between patients with HMCAS and those without (OR: 1.54, 95% CI: 0.24 to 9.66, p = .646); however, there was a substantial level of heterogeneity among the studies (I2 = 82%, p < .001). The test for overall effect further confirmed the lack of significant impact on the risk of sICH (Figure 3).
Figure 3.
Forest plot of symptomatic intracranial hemorrhage.
Successful recanalization
The analysis of five studies showed that successful recanalization rates were similar between HMCAS and non-HMCAS groups (OR = 1.23 (95% CI: 0.67 to 2.28 p = .501). However, the heterogeneity analysis revealed a moderate level of heterogeneity among the studies (I2 = 63%, p = .030) (Figure 4).
Figure 4.
Forest plot of successful recanalization (mTICI ≥ 2b).
In addition to meta-analysis, we presented two example cases depicting M1 occlusion scenarios, one with the presence of the hyperdense sign (HMCAS) and the other without. Figure 5 portrays a case with an M1 occlusion and the concomitant hyperdense sign. Following MT treatment, patient’s mTICI score was 2b and 90-day mRS score was 1. Figure 6 illustrates an M1 occlusion without the hyperdense sign, and patient’s symptoms completely improved after successful recanalization with mTICI 2c.
Figure 5.
A 45-year-old female patient who presented with complaints of right side weakness and aphasia. (a) The angiography image with a lateral view shows filling of the branches of the anterior cerebral artery, but no flow is observed in the left middle cerebral artery perfusion area (asterisk). (b) Within the first 90 min, the cranial CT scan showed a prominent hyperdense sign of the middle cerebral artery on the left side (arrow). After the patient underwent mechanical thrombectomy without any complications, the mTICI score was 2b and the 90-day mRS score was 1.
Figure 6.
A 57-year-old male patient who presented with complaints of left side facial droop and aphasia. (a) The angiography image with a lateral view shows filling of the branches of the anterior cerebral artery, but no flow is observed in the right middle cerebral artery perfusion area (asterisk). (b) In the cranial non-contrast CT scan, there was no hyperdense sign of the middle cerebral artery. Following mechanical thrombectomy, the patient’s mTICI score was 2c and 90-day mRS score was 0.
Discussion
Our meta-analysis comparing HMCAS to non-HMCAS MT revealed several key findings. Firstly, HMCAS and non-HMCAS groups had comparable successful recanalization and functional independence rates. Secondly, mortality and sICH rates did not significantly differ between the two groups. These findings suggest that HMCAS should be considered as a diagnostic clue for LVO rather than a prognostic marker.
While the diagnostic utility of HMCA is well known, its prognostic importance remains largely unexplored. Early clinical studies suggest that the presence of HMCAS is associated with poor clinical outcomes and an increased incidence of cerebral hemorrhage.3,19 However, it is important to note that these effects were partially influenced by the presence of other risk factors that were more prevalent in the HMCAS group. Furthermore, within the HMCAS subgroup, it was observed that individuals with a proximal and longer HMCAS had a higher likelihood of experiencing unfavorable outcomes. 3 Similarly, another study found that shorter HMCAS lengths (<10 mm) had a significantly higher rate of disappearance with intravenous tissue plasminogen activator compared to medium (10–20 mm) and long (>20 mm) lengths. 20 Conversely, Spiotta et al. showed that there were no significant correlations between clot length or density and recanalization, procedural complications, post-procedural hemorrhage, or functional outcomes at 90 days. While our meta-analysis did not include subgroup evaluations for HMCAS length, these additional studies emphasize the potential impact of HMCAS characteristics on treatment decision and response. 21 However, there was a lack of available prospective studies specifically focused on comparing HMCAS and non-HMCAS. In our meta-analysis, the odds ratio for successful recanalization was 1.59 (95% CI: 0.78 to 3.22). However, the observed differences in successful recanalization rates between HMCAS and non-HMCAS were not statistically significant, and there was a significant level of heterogeneity among the included studies.
The clinical outcomes of patients with HMCAS and non-HMCAS have been a subject of interest in stroke research. Although several studies have reported an association between HMCAS and poor outcomes,4–6 our meta-analysis did not find any significant superiorities in clinical outcomes between HMCAS and non-HMCAS groups. It is worth noting that HMCA is linked to an increased presence of red blood cells (RBCs) and a delicate clot structure. These factors could potentially hinder successful recanalization and result in unfavorable functional outcomes due to the risk of distal emboli. However, it is important to highlight that despite these potential drawbacks associated with HMCAS, our comprehensive meta-analysis did not find any significant impact on the rates of recanalization or favorable outcomes. The exact mechanisms underlying the association between HMCAS and poor clinical outcomes are not fully understood but may involve factors such as the extent of vessel occlusion, 2 collateral circulation status, 22 and ischemic injury severity. 5
The compromised blood flow and subsequent reperfusion injury following recanalization procedures may contribute to vessel wall disruption and subsequent bleeding.4,23 Moreover, the presence of a clot within the artery can disrupt the integrity of the vessel wall, making it more susceptible to hemorrhage. 24 However, our meta-analysis, which included four studies with 622 patients, did not find a statistically significant difference in the risk of symptomatic intracranial hemorrhage between patients with HMCAS and those without. The overall odds ratio from the random effects model was 1.54 (95% CI: 0.24 to 9.66), indicating no significant association. Despite this lack of statistical significance, it is crucial to remain vigilant for the possibility of symptomatic intracranial hemorrhage in patients with HMCAS due to the underlying pathophysiological mechanisms and the potential for adverse outcomes.
Our study has some limitations that should be considered. Firstly, the sample size was small, and most of the studies were conducted retrospectively, which limits the generalizability of the findings. Secondly, we only focused on the hyperdense MCA sign and did not consider other alternative signs, which may have resulted in overlooking relevant information. Thirdly, we lacked consistent data on the size and model of the thrombectomy devices used, as well as information on occlusion morphology, collateral status, and thrombolysis utilization.25,26 These factors could have influenced the treatment outcomes but were not adequately addressed in the included studies. Finally, we could not provide results on first pass efficacy and distal embolism as they were not reported in most of the included studies.
Conclusion
In conclusion, the findings from our meta-analysis suggest that HMCAS does not have a significant impact on mRS scores, mortality, or the risk of sICH. Further research is needed to fully understand the implications and establish the significance of these findings.
Supplemental Material
Supplemental Material for Outcomes of mechanical thrombectomy in M1 occlusion patients with or without hyperdense middle cerebral artery sign: A systematic review and meta-analysis by Atakan Orscelik, Yigit Can Senol, Cem Bilgin, Hassan Kobbeisi, Sherief Ghozy, Basel Musmar, Gokce Belge Bilgin, Sara Zandpazandi, Madonna Pakkam, Santhosh Arul, Waleed Brinjikji and David F Kallmes in The Neuroradiology Journal.
The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: W.B. holds equity in Nested Knowledge, Superior Medical Editors, Piraeus Medical, Sonoris Medical, and MIVI Neurovascular. He receives royalties from Medtronic and Balloon Guide Catheter Technology. He receives consulting fees from Medtronic, Stryker, Imperative Care, MicroVention, MIVI Neurovascular, Cerenovus, Asahi, and Balt. He serves in a leadership or fiduciary role for MIVI Neurovascular, Marblehead Medical LLC, Interventional Neuroradiology (Editor in Chief), Piraeus Medical, and WFITN. D.F.K. holds equity in Nested Knowledge, Superior Medical Editors, and Conway Medical, Marblehead Medical, and Piraeus Medical. He receives grant support from MicroVention, Medtronic, Balt, and Insera Therapeutics; has served on the Data Safety Monitoring Board for Vesalio; and received royalties from Medtronic.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
Supplemental Material: Supplemental material for this article is available online.
Ethical statement
Ethical approval
This study has been conducted in full accordance with ethical standards and has received approval from the Institutional Review Board (IRB: E1-21-1904) to ensure that it complies with ethical guidelines and safeguards the rights and well-being of the participants.
Informed consent
Prior to the inclusion of any patient data and imaging, informed consent was obtained from all participants involved in this study.
ORCID iDs
Atakan Orscelik https://orcid.org/0000-0001-6481-3076
Yigit Can Senol https://orcid.org/0000-0002-6669-6616
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Supplementary Materials
Supplemental Material for Outcomes of mechanical thrombectomy in M1 occlusion patients with or without hyperdense middle cerebral artery sign: A systematic review and meta-analysis by Atakan Orscelik, Yigit Can Senol, Cem Bilgin, Hassan Kobbeisi, Sherief Ghozy, Basel Musmar, Gokce Belge Bilgin, Sara Zandpazandi, Madonna Pakkam, Santhosh Arul, Waleed Brinjikji and David F Kallmes in The Neuroradiology Journal.