Abstract
Background
Mechanical thrombectomy (MT) is the treatment standard in eligible patients with acute ischemic stroke (AIS) secondary to large vessel occlusions (LVO). Studies have shown that good collateral status is a strong predictor of MT efficacy, thus making collateral status important to quickly assess. The Los Angeles Motor Scale is a clinically validated tool for identifying LVO in the field. The aim of this study is to investigate whether admission LAMS score is also associated with the American Society of Interventional and Therapeutic Neuroradiology (ASITN) collateral score on digital subtraction angiography (DSA).
Methods
We conducted a retrospective multicenter cohort study of consecutive patients presenting with AIS caused by LVO from 9/1/2017 to 10/1/2023 with diagnostically adequate DSA imaging. Demographic, clinical, and imaging data was collected through manual chart review. Both univariate and multivariate analysis were applied to assess associations. A p-value <0.05 was considered significant.
Results
A total of 308 patients (median age: 68, IQR: 57.5–77) were included in the study. On multivariate logistic regression analysis, we found that lower admission LAMS score (adjusted OR: 0.82, 95% CI: 0.68–0.98, p < 0.05) and higher ASPECTS score (adjusted OR: 1.21, 95% CI: 1.02–1.42, p < 0.05) were independently associated with good DSA ASITN collateral score of 3-4.
Conclusions
Admission LAMS and ASPECTS score are both independently associated with DSA ASITN collateral score. This demonstrates the capability of LAMS to act as a surrogate marker of CS in the field.
Keywords: Stroke, large vessel occlusion, mechanical thrombectomy, collateral status, Los Angeles motor scale
Introduction
Acute ischemic stroke secondary to large vessel occlusion (AIS-LVO) is a leading cause of morbidity and mortality in the United States. 1 In eligible patients, mechanical thrombectomy (MT) is the standard of treatment for AIS-LVO.2,3 A clinically validated tool for quickly identifying patients with LVO on the field outside of hospital setting is the Los Angeles Motor Scale (LAMS), which is a 5 point scale based on stroke severity.4–6 Through its use, medical personnel can identify stroke patients with LVO who may be eligible for MT prior to arriving at the hospital.
Collateral status (CS), or the presence of robust collateral blood flow, is a key determinant of MT efficacy. Previous studies have shown that patients with better CS have superior post-MT outcomes, including smaller infarct growth, greater penumbra salvage, and improved functional outcomes.7–10 Conversely, in patients with poor collateral status, MT may have little to no effect. While there are several methods of estimating a patient's CS, the gold standard is the digital subtraction angiograph (DSA)-derived American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology (ASITN/SIR) collateral score, otherwise known as the DSA ASITN score. The DSA ASITN score assigns a grade of 0 to 4 depending on the quality of the collateral status, with grade 0 representing no collateral blood flow and grade 4 representing complete and rapid collateral blood flow to the ischemic area. 11 DSA ASITN grades of 3-4 are considered good collateral status and have been associated with superior post-MT outcomes.10,12–14
Although LAMS is a well-established marker for LVO estimation, less is known about its relationship to CS. Given the importance of CS in determining the efficacy of MT treatment, it is of great interest to know if LAMS can also provide information on a patient's CS, which would further improve its utility in identifying suitable candidates for MT. Hence, this study aims to investigate the relationship between admission LAMS with DSA ASITN collateral scores.
Methods
Study design
We performed a retrospective, multicenter analysis of prospectively maintained stroke databases and identified consecutive patients from September 01, 2017 to October 01, 2023 who met our inclusion criteria. This study was approved through the institutional review board (protocol code JHU-IRB00269637) and follows the STROBE checklist guidelines as an observational study. 15
Study participants
The inclusion criteria for this study were patients with (1) AIS due to a CTA-confirmed LVO of the intracranial ICA supraclinoid segment, M1 segment of the MCA, or proximal M2 segment of the MCA; 16 and (2) diagnostically adequate pretreatment DSA imaging.
The study was conducted in accordance with the Declaration of Helsinki and the Health Insurance Portability and Accountability Act (HIPAA). Informed consent was waived by the institutional review boards given the retrospective study design. The decisions to administer IV thrombolysis and/or perform MT were made on an individual basis based on consensus stroke team evaluation per institutional protocols.
Data collection
Baseline and clinical data were collected through a review of electronic medical records and stroke center databases. Data collected for each patient included demographics, site of occlusion, interventional data, premorbid modified Rankin scores, baseline CT parameters, and pre-treatment DSA ASITN collateral scores.
LAMS score assessment
The LAMS score is a 5-point scale that is calculated based on the presence or absence of facial droop, arm weakness, and grip weakness. Starting from a score of zero, presence of facial droop adds one point; arm drifting down slowly adds one point, while arm drifting down rapidly adds two points; and weak grip strength adds one point, while absent grip strength adds two points.
DSA image acquisition and analysis
The ASITN CS was independently assessed by a board-certified neuroradiologist and the performing neuro-interventionalist. Any discrepancies were resolved based on a consensus review. ASITN grades included the following: Grade 0, defined as no collaterals visible to the ischemic region; Grade 1, defined as slow collaterals to the periphery with persisting defect; Grade 2, defined as rapid collaterals to the periphery with persisting defect; Grade 3, defined as slow-but-complete collateral flow to the ischemic territory; and Grade 4, defined as rapid and complete collateral flow to the ischemic territory.17–19
Statistical analysis
Multivariable logistic regression analysis adjusting for age, sex, race, hypertension, hyperlipidemia, diabetes mellitus, heart disease, prior stroke or TIA, premorbid mRS, admission NIHSS, and ASPECTS score was used to assess the association of admission LAMS with DSA ASITN collateral score. The outcomes were dichotomized into nominal variables for logistic regression analysis; DSA ASITN score of 0–2 was considered poor collateral status and DSA ASITN score of 3-4 was considered good collateral status, based on current literature. A p-value of <0.05 was considered significant.
Results
A total of 308 consecutive patients were included in the study. The median age of the study population was 68 years (IQR: 57.5–77), with 172 (56%) of the participants being female and 136 (44%) of the participants being male. Of the study participants, 167 (54%) had a LAMS score of 3-4. Patient demographic details are presented in Table 1.
Table 1.
Demographics, imaging characteristics, and interventional parameters of study participants.
| Characteristics | Admission LAMS 4-5 (n = 167) | Admission LAMS 0-3 (n = 141) | Total (n = 308) | p-value | ||||
|---|---|---|---|---|---|---|---|---|
| Number/Median | %/IQR | Number/Median | %/IQR | Number/Median | %/IQR | |||
| Age | 68 | 60–78 | 67 | 57–77 | 68 | 57.5–77 | 0.79 | |
| Sex | Male | 68 | 40.7% | 68 | 48.2% | 136 | 44.2% | 0.19 |
| Female | 99 | 59.3% | 73 | 51.8% | 172 | 55.8% | ||
| Race | African | 62 | 37.1% | 62 | 44.0% | 124 | 40.3% | 0.17 |
| Caucasian | 96 | 57.5% | 67 | 47.5% | 163 | 52.9% | ||
| Asian | 2 | 1.2% | 6 | 4.3% | 8 | 2.6% | ||
| Others | 7 | 4.2% | 6 | 4.3% | 13 | 4.2% | ||
| Smoking | 78 | 47.9% | 61 | 44.2% | 139 | 46.2% | 0.85 | |
| Alcohol | 51 | 31.5% | 41 | 29.7% | 92 | 30.7% | 0.74 | |
| Hypertension | 135 | 80.8% | 104 | 73.8% | 239 | 77.6% | 0.14 | |
| Hyperlipidemia | 89 | 53.9% | 73 | 52.1% | 162 | 53.1% | 0.75 | |
| Diabetes | 41 | 24.7% | 37 | 26.4% | 78 | 25.5% | 0.73 | |
| Heart Disease | 89 | 53.9% | 74 | 52.9% | 163 | 53.4% | 0.85 | |
| Prior stroke or TIA | 38 | 23.0% | 26 | 18.6% | 64 | 21.0% | 0.34 | |
| IV tPA Administration | 61 | 38.9% | 50 | 36.8% | 111 | 37.9% | 0.71 | |
| Symptom Onset to Door Time (minutes) | 66 | 41–127 | 66.5 | 46–111 | 66 | 44–125 | 0.47 | |
| Door to Needle Time (minutes) | 59.5 | 47–78.5 | 56.5 | 38–84 | 58 | 41–82 | 0.28 | |
| Door to Groin Puncture Time (minutes) | 148.5 | 119.5–214.5 | 171 | 126–246 | 154 | 126–222 | 0.21 | |
| Premorbid mRS | 0 | 101 | 62.7% | 102 | 72.9% | 203 | 67.4% | 0.12 |
| 1 | 29 | 18.0% | 11 | 7.9% | 40 | 13.3% | ||
| 2 | 14 | 8.7% | 11 | 7.9% | 25 | 8.3% | ||
| 3 | 15 | 9.3% | 15 | 10.7% | 30 | 10.0% | ||
| 4 | 2 | 1.2% | 1 | 0.7% | 3 | 1.0% | ||
| 5 | 0 | 0.0% | 0 | 0.0% | 0 | 0.0% | ||
| 6 | 0 | 0.0% | 0 | 0.0% | 0 | 0.0% | ||
| Occlusion Site | M1 | 111 | 66.5% | 113 | 80.1% | 224 | 72.7% | <0 . 05 |
| Proximal M2 | 40 | 24.0% | 20 | 14.2% | 60 | 19.5% | ||
| Supraclinoid ICA | 16 | 9.6% | 8 | 5.7% | 24 | 7.8% | ||
| ASPECTS Score | 0 | 1 | 0.6% | 1 | 0.7% | 2 | 0.7% | 0.84 |
| 1 | 0 | 0.0% | 0 | 0.0% | 0 | 0.0% | ||
| 2 | 0 | 0.0% | 0 | 0.0% | 0 | 0.0% | ||
| 3 | 5 | 3.0% | 2 | 1.4% | 7 | 2.3% | ||
| 4 | 1 | 0.6% | 1 | 0.7% | 2 | 0.7% | ||
| 5 | 7 | 4.2% | 3 | 2.1% | 10 | 3.3% | ||
| 6 | 11 | 6.7% | 8 | 5.7% | 19 | 6.2% | ||
| 7 | 13 | 7.9% | 15 | 10.6% | 28 | 9.2% | ||
| 8 | 25 | 15.2% | 16 | 11.3% | 41 | 13.4% | ||
| 9 | 25 | 15.2% | 20 | 14.2% | 45 | 14.7% | ||
| 10 | 77 | 46.7% | 75 | 53.2% | 152 | 49.7% | ||
| Tan Score | 0 | 22 | 14.1% | 6 | 4.5% | 28 | 9.7% | <0 . 01 |
| 1 | 43 | 27.6% | 53 | 40.2% | 96 | 33.3% | ||
| 2 | 74 | 47.4% | 54 | 40.9% | 128 | 44.4% | ||
| 3 | 17 | 10.9% | 19 | 14.4% | 36 | 12.5% | ||
| rCBF < 30% Lesion Volume (Dichotomous) | >50 mL (large core) | 22 | 19.0% | 14 | 13.2% | 36 | 16.2% | |
| <50 mL (small core) | 94 | 81.0% | 92 | 86.8% | 186 | 83.8% | ||
| rCBF < 30% Lesion Volume (Continuous) | 6 | 0–35.5 | 5.5 | 0–25 | 6 | 0–28 | 0.25 | |
| Tmax < 6 s Lesion Volume | 110 | 62.5–155 | 120.5 | 76–163 | 111.5 | 67–159 | 0.63 | |
| DSA ASITN Collateral Score | 0 | 24 | 14.4% | 12 | 8.5% | 36 | 11.7% | 0.45 |
| 1 | 42 | 25.1% | 37 | 26.2% | 79 | 25.6% | ||
| 2 | 49 | 29.3% | 46 | 32.6% | 95 | 30.8% | ||
| 3 | 41 | 24.6% | 32 | 22.7% | 73 | 23.7% | ||
| 4 | 11 | 6.6% | 14 | 9.9% | 25 | 8.1% | ||
Bold represents statistically significant values.
Logistic regression analysis showed that admission NIHSS score (unadjusted OR: 0.96, 95% CI: 0.93–0.99, p < 0.05), ASPECTS score (unadjusted OR: 1.24, 95% CI: 1.06–1.45, p-value < 0.001), and admission LAMS score (unadjusted OR: 0.78, 95% CI: 0.67–0.91, p < 0.01) were associated with good DSA ASITN collateral score of 3-4. When adjusting for cofounding variables, we found that lower admission LAMS score (adjusted OR: 0.82, 95% CI: 0.68–0.98, p < 0.05) and higher ASPECTS score (adjusted OR: 1.21, 95% CI: 1.02–1.42, p < 0.05) were independently associated with good DSA ASITN collateral score of 3-4. Results of the regression analysis are presented in Table 2.
Table 2.
Logistic regression analysis of studied variables in predicting DSA ASITN collateral scores, dichotomized into a nominal variable using scores > 2 as the cutoff.
| Variable | Univariable Analysis | Multivariable Analysis | ||||||
|---|---|---|---|---|---|---|---|---|
| Unadjusted OR | 95% Confidence Interval | p-value | Unadjusted OR | 95% Confidence Interval | p-value | |||
| Lower | Upper | Lower | Upper | |||||
| Age | 1.00 | 0.98 | 1.01 | 0.59 | 1.00 | 0.98 | 1.02 | 0.74 |
| Sex | 0.77 | 0.47 | 1.25 | 0.29 | 0.78 | 0.46 | 1.33 | 0.37 |
| Race | 0.99 | 0.71 | 1.38 | 0.95 | 0.94 | 0.64 | 1.36 | 0.72 |
| Hypertension | 0.77 | 0.44 | 1.36 | 0.37 | 0.69 | 0.36 | 1.33 | 0.27 |
| Hyperlipidemia | 1.09 | 0.67 | 1.77 | 0.72 | 1.07 | 0.63 | 1.82 | 0.80 |
| Diabetes Mellitus | 1.11 | 0.64 | 1.91 | 0.72 | 1.13 | 0.61 | 2.10 | 0.69 |
| Heart Disease | 1.01 | 0.62 | 1.64 | 0.97 | 0.95 | 0.55 | 1.62 | 0.85 |
| Prior Stroke or TIA | 1.06 | 0.59 | 1.91 | 0.85 | 0.96 | 0.50 | 1.84 | 0.89 |
| Premorbid mRS | 1.17 | 0.94 | 1.46 | 0.16 | 1.24 | 0.95 | 1.60 | 0.11 |
| Admission NIHSS | 0.96 | 0.93 | 0.99 | <0 . 05 | 0.97 | 0.93 | 1.01 | 0 . 17 |
| ASPECTS | 1.24 | 1.06 | 1.45 | <0 . 001 | 1.21 | 1.02 | 1.42 | <0 . 05 |
| Admission LAMS | 0.78 | 0.67 | 0.91 | <0 . 01 | 0.82 | 0.68 | 0.98 | <0 . 05 |
Bold represents statistically significant values.
Conclusions
In this study, we aimed to determine the relationship between admission LAMS and the DSA ASITN score, which is considered the reference standard for CS assessment. Our results demonstrate that admission LAMS and ASPECTS score are both independent predictors of a good DSA ASITN collateral score.
DSA ASITN collateral scores are the gold standard for assessing a patient's collateral status (CS). It has been extensively demonstrated that good CS (DSA ASITN scores of 3-4) is associated with superior post-thrombectomy outcomes in patients with acute ischemic stroke from large vessel occlusion.7–10,12–14 Similarly, it has been demonstrated that poor CS (DSA ASITN scores of 0–2) is associated with increased risk of post-procedural complications and less favorable outcomes.20–22 Thus, being able to quickly determine a patient's CS is pivotal in guiding interventional management. Given the speed that LAMS can be performed even prior to arriving at a medical center, it is of great interest to know whether it can also help predict CS. A previous paper showed an association between admission LAMS with CT perfusion collateral status parameters. 23 To our knowledge, our study is the first to describe the association between admission LAMS with DSA ASITN collateral scores.
In our study, a lower admission LAMS was independently associated with a good DSA ASITN collateral score (adjusted OR: 0.82, 95% CI: 0.68–0.98, p < 0.05). This suggests that reduced stroke symptom severity is associated with better CS. One likely explanation for this is that patients with better CS can maintain a greater level of perfusion to the affected brain tissue after an ischemic event, resulting in greater preservation of motor function by time of evaluation.24,25 It is also possible that patients with better baseline CS are more likely to have other neuroprotective factors that can mitigate the clinical severity of a stroke. For example, patients with better baseline CS may have more baseline pro-angiogenic factors, enabling greater perfusion to the affected brain tissue after an acute stroke and thus a lower LAMS score.26–28 Ultimately, we show that LAMS is useful in not only identifying LVO candidates for mechanical thrombectomy, but also providing insight into their collateral status and thus the possible effectiveness of the therapy. Our finding further supports the effectiveness of LAMS as an early stroke triaging tool.
Our study also found that higher baseline, pre-treatment ASPECTS score on NCCT was an independent predictor of good DSA ASITN collateral scores (adjusted OR: 1.21, 95% CI: 1.02–1.42, p < 0.05). This aligns with previous findings that collateral status and ASPECTS score are positively correlated.24,29 The ASPECTS score is a score from 0 to 10 that represents an estimation of the extent of brain tissue affected by an MCA stroke, with higher scores indicating less involvement. 30 A reasonable theory is that patients with superior CS sustain perfusion of a larger area of brain tissue after a stroke and thus achieve a higher ASPECTS score.
There are several study design limitations that should be considered when interpreting these results. First, the retrospective study design inherently limits the study. We aimed to minimize this by only including consecutive patients from two comprehensive stroke centers within our larger hospital enterprise. Second, the LAMS scores were self-adjudicated by the responding medical personnel, and thus may not be completely standardized. However, all LAMS scores used in the study were adjudicated by experienced medical personnel within the same hospital system. Third, our study only includes patients with confirmed LVOs. Unfortunately, this information is not available when using the LAMS score to make the triage decision in the field, and thus our findings may not reflect the full scope of stroke patients for whom LAMS is applied. Additional prospective studies should be conducted to further elucidate the association between LAMS and collateral status.
In conclusion, we report that admission LAMS and ASPECTS score are independently associated with DSA ASITN collateral score. This demonstrates the capability of LAMS to act as a surrogate marker of CS in the field. Ultimately, LAMS may aid in the early triage of stroke patients and the decision to route them to thrombectomy capable centers.
Acknowledgments
The work has been accomplished with the support of the Johns Hopkins University School of Medicine Department of Radiology Physician Scientist Incubator Program.
Footnotes
Author contributions: R.W. and D.A.L. contributed equally to this work.
Consent to participate: Informed consent was waived by the institutional review boards given the retrospective study design.
Consent for publication: Not Applicable
Data availability: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Declaration of conflicting interest: The authors do not have any conflict of interest to disclose except for Dr. Vivek Yedavalli, who serves as a consultant for MRIOnline (Cincinnati, OH, USA), RAPID (IschemaView, Menlo Park, CA, USA), and editorial board of Frontiers in Radiology.
Ethical approval and informed consent statement: This study was approved through the institutional review board (protocol code JHU-IRB00269637) and follows the STROBE checklist guidelines as an observational study.
The study was conducted in accordance with the Declaration of Helsinki and the Health Insurance Portability and Accountability Act (HIPAA). Informed consent was waived by the institutional review boards given the retrospective study design. The decisions to administer IV thrombolysis and/or perform MT were made on an individual basis based on consensus stroke team evaluation per institutional protocols.
Funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
ORCID iDs: Richard Wang https://orcid.org/0000-0003-3442-0559
Dhairya A Lakhani https://orcid.org/0000-0001-7577-1887
Manisha Koneru https://orcid.org/0000-0001-5012-6793
Vivek S Yedavalli https://orcid.org/0000-0002-2450-4014
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