The Effects of Carotid Pathologies on Short-Term Functional Outcomes After First-Ever Small Vessel Occlusion Stroke
Abstract
1. Introduction
2. Materials and Methods
2.1. Patient Inclusion
2.2. Carotid Assessments
2.3. Functional Outcome and Covariates
2.4. Statistical Analysis
3. Results
3.1. Baseline Characteristics
3.2. Logistic Regression Models
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
SVO | small vessel occlusion |
CIMT | carotid intima–media thickness |
mRS | modified Rankin scale |
FI | functional independence |
FD | functional dependence |
NIHSS | National Institutes of Health Stroke Scale |
OR | odds ratio |
CI | confidence interval |
References
- Rathburn, C.M.; Mun, K.T.; Sharma, L.K.; Saver, J.L. TOAST stroke subtype classification in clinical practice: Implications for the Get with the Guidelines-Stroke nationwide registry. Front. Neurol. 2024, 15, 1375547. [Google Scholar] [CrossRef] [PubMed]
- Arboix, A.; Marti-Vilalta, J.L. Lacunar stroke. Expert. Rev. Neurother. 2009, 9, 179–196. [Google Scholar] [CrossRef] [PubMed]
- Guan, Y.; Yu, C.; Zuo, W.; Jia, K.; Liu, F.; Lu, H.; Wang, X.; Wang, D.; Wang, X. Factors associated with prognosis after small-vessel occlusion among young and middle-aged patients: A hospital-based follow-up study. Postgrad. Med. 2021, 133, 581–586. [Google Scholar] [CrossRef] [PubMed]
- Kalaria, R.N.; Akinyemi, R.; Ihara, M. Stroke injury, cognitive impairment and vascular dementia. Biochim. Biophys. Acta 2016, 1862, 915–925. [Google Scholar] [CrossRef] [PubMed]
- van Sloten, T.T.; Sedaghat, S.; Laurent, S.; London, G.M.; Pannier, B.; Ikram, M.A.; Kavousi, M.; Mattace-Raso, F.; Franco, O.H.; Boutouyrie, P.; et al. Carotid stiffness is associated with incident stroke: A systematic review and individual participant data meta-analysis. J. Am. Coll. Cardiol. 2015, 66, 2116–2125. [Google Scholar] [CrossRef] [PubMed]
- Miceli, G.; Basso, M.G.; Pintus, C.; Pennacchio, A.R.; Cocciola, E.; Cuffaro, M.; Profita, M.; Rizzo, G.; Tuttolomondo, A. Molecular pathways of vulnerable carotid plaques at risk of ischemic stroke: A narrative review. Int. J. Mol. Sci. 2024, 25, 4351. [Google Scholar] [CrossRef] [PubMed]
- van Dijk, A.C.; Fonville, S.; Zadi, T.; van Hattem, A.M.; Saiedie, G.; Koudstaal, P.J.; van der Lugt, A. Association between arterial calcifications and nonlacunar and lacunar ischemic strokes. Stroke 2014, 45, 728–733. [Google Scholar] [CrossRef] [PubMed]
- Lu, T.; Liang, J.; Wei, N.; Pan, L.; Yang, H.; Weng, B.; Zeng, J. Extracranial artery stenosis is associated with total MRI burden of cerebral small vessel disease in ischemic stroke patients of suspected small or large artery origins. Front. Neurol. 2019, 10, 243. [Google Scholar] [CrossRef] [PubMed]
- Humayra, S.; Yahya, N.; Ning, C.J.; Raffali, M.; Mir, I.A.; Mohamed, A.L.; Manan, H.A. Relationship between carotid intima-media thickness and white matter hyperintensities in non-stroke adults: A systematic review. Front. Neuroanat. 2024, 18, 1394766. [Google Scholar] [CrossRef] [PubMed]
- Della-Morte, D.; Dong, C.; Markert, M.S.; Elkind, M.S.V.; Sacco, R.L.; Wright, C.B.; Rundek, T. Carotid intima-media thickness is associated with white matter hyperintensities: The Northern Manhattan Study. Stroke 2018, 49, 304–311. [Google Scholar] [CrossRef] [PubMed]
- Jeong, H.Y.; Jung, K.H.; Mo, H.; Lee, C.H.; Kim, T.J.; Park, J.M.; Oh, M.; Lee, J.S.; Kim, B.J.; Kim, J.T.; et al. Characteristics and management of stroke in Korea: 2014-2018 data from Korean Stroke Registry. Int. J. Stroke 2020, 15, 619–626. [Google Scholar] [CrossRef] [PubMed]
- Adams, H.P., Jr.; Bendixen, B.H.; Kappelle, L.J.; Biller, J.; Love, B.B.; Gordon, D.L.; Marsh, E.E., 3rd. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 1993, 24, 35–41. [Google Scholar] [CrossRef] [PubMed]
- Fernandez-Alvarez, V.; Linares Sanchez, M.; Lopez Alvarez, F.; Suarez Nieto, C.; Makitie, A.A.; Olsen, K.D.; Ferlito, A. Evaluation of intima-media thickness and arterial stiffness as early ultrasound biomarkers of carotid artery atherosclerosis. Cardiol. Ther. 2022, 11, 231–247. [Google Scholar] [CrossRef] [PubMed]
- Johri, A.M.; Nambi, V.; Naqvi, T.Z.; Feinstein, S.B.; Kim, E.S.H.; Park, M.M.; Becher, H.; Sillesen, H. Recommendations for the assessment of carotid arterial plaque by ultrasound for the characterization of atherosclerosis and evaluation of cardiovascular risk: From the American Society of Echocardiography. J. Am. Soc. Echocardiogr. 2020, 33, 917–933. [Google Scholar] [CrossRef] [PubMed]
- Pruissen, D.M.; Gerritsen, S.A.; Prinsen, T.J.; Dijk, J.M.; Kappelle, L.J.; Algra, A.; Group, S.S. Carotid intima-media thickness is different in large- and small-vessel ischemic stroke: The SMART study. Stroke 2007, 38, 1371–1373. [Google Scholar] [CrossRef] [PubMed]
- Burke, M.J.; Vergouwen, M.D.; Fang, J.; Swartz, R.H.; Kapral, M.K.; Silver, F.L.; Casaubon, L.K.; Investigators of the Registry of the Canadian Stroke Network. Short-term outcomes after symptomatic internal carotid artery occlusion. Stroke 2011, 42, 2419–2424. [Google Scholar] [CrossRef] [PubMed]
- Leng, X.Y.; Chen, X.Y.; Chook, P.; Xiong, L.; Lin, W.H.; Liu, J.Y.; Tomlinson, B.; Thomas, G.N.; Lam, T.H.; Lam, K.S.; et al. Correlation of large artery intracranial occlusive disease with carotid intima-media thickness and presence of carotid plaque. Stroke 2013, 44, 68–72. [Google Scholar] [CrossRef] [PubMed]
- Johansson, E.; Cuadrado-Godia, E.; Hayden, D.; Bjellerup, J.; Ois, A.; Roquer, J.; Wester, P.; Kelly, P.J. Recurrent stroke in symptomatic carotid stenosis awaiting revascularization: A pooled analysis. Neurology 2016, 86, 498–504. [Google Scholar] [CrossRef] [PubMed]
- Roy-O’Reilly, M.; McCullough, L.D. Age and sex are critical factors in ischemic stroke pathology. Endocrinology 2018, 159, 3120–3131. [Google Scholar] [CrossRef] [PubMed]
- Katzan, I.L.; Spertus, J.; Bettger, J.P.; Bravata, D.M.; Reeves, M.J.; Smith, E.E.; Bushnell, C.; Higashida, R.T.; Hinchey, J.A.; Holloway, R.G.; et al. Risk adjustment of ischemic stroke outcomes for comparing hospital performance: A statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2014, 45, 918–944. [Google Scholar] [CrossRef] [PubMed]
- Kasner, S.E. Clinical interpretation and use of stroke scales. Lancet Neurol. 2006, 5, 603–612. [Google Scholar] [CrossRef] [PubMed]
- Lee, K.B.; Kim, J.S.; Hong, B.Y.; Lim, S.H. Clinical recovery from stroke lesions and related outcomes. J. Clin. Neurosci. 2017, 37, 79–82. [Google Scholar] [CrossRef] [PubMed]
- Schiemanck, S.K.; Kwakkel, G.; Post, M.W.; Kappelle, L.J.; Prevo, A.J. Impact of internal capsule lesions on outcome of motor hand function at one year post-stroke. J. Rehabil. Med. 2008, 40, 96–101. [Google Scholar] [CrossRef] [PubMed]
- Ntaios, G.; Milionis, H.; Vemmos, K.; Makaritsis, K.; Ferrari, J.; Strbian, D.; Curtze, S.; Tatlisumak, T.; Michel, P.; Papavasileiou, V. Small-vessel occlusion versus large-artery atherosclerotic strokes in diabetics: Patient characteristics, outcomes, and predictors of stroke mechanism. Eur. Stroke J. 2016, 1, 108–113. [Google Scholar] [CrossRef] [PubMed]
- Jiang, C.; Zhang, J.; Zhu, J.; Wang, X.; Wen, Z.; Zhao, X.; Yuan, C.; Investigators, C.-I. Association between coexisting intracranial artery and extracranial carotid artery atherosclerotic diseases and ipsilateral cerebral infarction: A Chinese Atherosclerosis Risk Evaluation (CARE-II) study. Stroke Vasc. Neurol. 2021, 6, 595–602. [Google Scholar] [CrossRef] [PubMed]
- Zafar, A. Diabetic patients are at a higher risk of lacunar infarction and dyslipidemia: Results of a comparative pilot study from King Fahad Hospital of the University, Saudi Arabia. Neurosciences 2017, 22, 20–24. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Liu, Y.; Liu, S.; Gao, M.; Wang, W.; Chen, K.; Huang, L.; Liu, Y. Diabetic vascular diseases: Molecular mechanisms and therapeutic strategies. Signal Transduct. Target. Ther. 2023, 8, 152. [Google Scholar] [CrossRef] [PubMed]
- Bartman, W.; Nabrdalik, K.; Kwiendacz, H.; Sawczyn, T.; Tomasik, A.; Pierzchala, K.; Adamczyk-Sowa, M.; Machowska-Majchrzak, A.; Labuz-Roszak, B.; Grzeszczak, W.; et al. Association between carotid plaque score and microvascular complications of type 2 diabetes. Pol. Arch. Intern. Med. 2017, 127, 418–422. [Google Scholar] [CrossRef] [PubMed]
- Grant, E.G.; Benson, C.B.; Moneta, G.L.; Alexandrov, A.V.; Baker, J.D.; Bluth, E.I.; Carroll, B.A.; Eliasziw, M.; Gocke, J.; Hertzberg, B.S.; et al. Carotid artery stenosis: Gray-scale and Doppler US diagnosis—Society of Radiologists in Ultrasound Consensus Conference. Radiology 2003, 229, 340–346. [Google Scholar] [CrossRef] [PubMed]
Variables | FI Group (n = 276) | FD Group (n = 96) | p-Value |
---|---|---|---|
Age, years | 66.6 ± 11.6 | 72.6 ± 11.7 | <0.001 |
Male, n (%) | 93 (33.7) | 51 (53.1) | 0.001 |
Onset to arrival, days | 2.8 ± 22.1 | 1.2 ± 1.4 | 0.229 |
NIHSS at initial presentation | 1.7 ± 1.7 | 4.5 ± 3.2 | <0.001 |
Previous mRS, n (%) | 0.979 | ||
0 | 274 (99.3) | 96 (100.0) | |
1 | 2 (0.7) | 0 (0.0) | |
Admission route, n (%) | 0.022 | ||
Outpatient clinic | 18 (6.5) | 0 (0.0) | |
Emergency department | 258 (93.5) | 96 (100.0) | |
Ward type, n (%) | 0.014 | ||
General ward | 59 (21.4) | 9 (9.4) | |
Stroke care unit | 217 (78.6) | 87 (90.6) | |
Abdominal circumference, cm | 84.7 ± 9.3 | 85.9 ± 10.3 | 0.277 |
Body mass index, kg/m2 | 23.9 ± 3.0 | 24.1 ± 4.1 | 0.739 |
Side of the stroke lesion, n (%) | 0.750 | ||
Right | 122 (44.7) | 47 (49.0) | |
Left | 137 (50.2) | 45 (46.9) | |
Bilateral | 14 (5.1) | 4 (4.2) | |
Lesion location, n (%) | 0.003 | ||
Basal ganglia | 35 (13.0) | 17 (17.7) | |
Thalamic | 40 (14.8) | 3 (3.1) | |
Cortical area | 30 (11.1) | 7 (7.3) | |
Corona radiata | 68 (25.2) | 39 (40.6) | |
Posterior circulation area | 67 (24.8) | 17 (17.7) | |
Multiple area | 30 (11.1) | 13 (13.5) | |
Comorbidities, n (%) | |||
Coronary artery diseases | 28 (10.1) | 11 (11.5) | 0.866 |
Atrial fibrillation | 13 (4.7) | 5 (5.2) | 1.000 |
Hypertension | 159 (57.6) | 57 (59.4) | 0.856 |
Diabetes | 78 (28.3) | 35 (36.5) | 0.169 |
Dyslipidemia | 245 (88.8) | 85 (88.5) | 1.000 |
Previous antiplatelet therapy | 32 (11.6) | 21 (21.9) | 0.021 |
Ejection fraction, % | 60.1 ± 3.8 | 59.3 ± 5.1 | 0.164 |
Carotid plaque grade 1, n (%) | 0.016 | ||
Normal | 29 (12.0) | 7 (7.7) | |
Grade I | 36 (14.9) | 9 (9.9) | |
Grade II | 98 (40.5) | 28 (30.8) | |
Grade III | 79 (32.6) | 47 (51.6) | |
Mean carotid intimal thickness 1, mm | 0.7 ± 0.1 | 0.7 ± 0.1 | 0.060 |
NIHSS at discharge | 0.5 ± 0.9 | 3.3 ± 2.6 | <0.001 |
Variables | Odds Ratio | 95% CI | p-Value |
---|---|---|---|
Mean carotid intimal thickness (per 1 SD) | 1.23 | 0.97–1.56 | 0.084 |
Carotid plaque grade 1 | |||
Normal | Reference | ||
Grade I | 1.04 | 0.34–3.22 | 0.950 |
Grade II | 1.18 | 0.49–3.19 | 0.721 |
Grade III | 2.46 | 1.05–6.51 | 0.049 |
Variables | Adjusted OR | 95% CI | p-Value |
---|---|---|---|
Carotid plaque grade 1 | |||
Normal | Reference | ||
Grade I | 0.07 | 0.35–3.42 | 0.906 |
Grade II | 1.06 | 0.41–2.98 | 0.913 |
Grade III | 2.07 | 0.80–5.91 | 0.149 |
Age (years) | 1.03 | 1.00–1.05 | 0.047 |
Sex (male) | 2.31 | 1.36–3.97 | 0.002 |
Variables | Adjusted OR | 95% CI | p-Value |
---|---|---|---|
Age (years) | 1.07 | 1.03–1.10 | <0.001 |
Sex (male) | 0.48 | 0.24–0.93 | 0.030 |
NIHSS at initial presentation | 1.84 | 1.55–2.18 | <0.001 |
Ward type (stroke unit care) | 0.56 | 0.59–4.13 | 0.376 |
Body mass index (per 1 kg/m2) | 1.05 | 0.96–1.16 | 0.267 |
Lesion location | |||
Basal ganglia | Reference | ||
Thalamic | 0.14 | 0.03–0.79 | 0.026 |
Cortical area | 1.12 | 0.27–4.68 | 0.878 |
Corona radiata | 1.13 | 0.44–2.91 | 0.796 |
Posterior circulation area | 0.51 | 0.17–1.49 | 0.220 |
Multiple area | 0.63 | 0.18–2.16 | 0.462 |
Ejection fraction (per 1%) | 0.98 | 0.90–1.07 | 0.625 |
Comorbidities | |||
Coronary artery diseases | 1.43 | 0.52–3.93 | 0.484 |
Atrial fibrillation | 0.68 | 0.15–3.04 | 0.613 |
Hypertension | 0.56 | 0.28–1.13 | 0.104 |
Diabetes | 2.84 | 1.37–5.92 | 0.005 |
Dyslipidemia | 1.33 | 0.46–3.86 | 0.596 |
Previous antiplatelet therapy | 1.59 | 0.65–3.88 | 0.305 |
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Bae, M.; Jeong, Y.-S.; Phoung, S.; Borei, P.; Koo, D.; Park, D. The Effects of Carotid Pathologies on Short-Term Functional Outcomes After First-Ever Small Vessel Occlusion Stroke. Brain Sci. 2025, 15, 773. https://doi.org/10.3390/brainsci15070773
Bae M, Jeong Y-S, Phoung S, Borei P, Koo D, Park D. The Effects of Carotid Pathologies on Short-Term Functional Outcomes After First-Ever Small Vessel Occlusion Stroke. Brain Sciences. 2025; 15(7):773. https://doi.org/10.3390/brainsci15070773
Chicago/Turabian StyleBae, Minwook, Yong-Suk Jeong, Sopheak Phoung, Phoeuk Borei, Dahyeon Koo, and Dougho Park. 2025. "The Effects of Carotid Pathologies on Short-Term Functional Outcomes After First-Ever Small Vessel Occlusion Stroke" Brain Sciences 15, no. 7: 773. https://doi.org/10.3390/brainsci15070773
APA StyleBae, M., Jeong, Y.-S., Phoung, S., Borei, P., Koo, D., & Park, D. (2025). The Effects of Carotid Pathologies on Short-Term Functional Outcomes After First-Ever Small Vessel Occlusion Stroke. Brain Sciences, 15(7), 773. https://doi.org/10.3390/brainsci15070773