Hesna BEKTAŞ, Esra DEMİR ÜNAL, Oğuzhan KURŞUN, Hasan BAYINDIR

Bio-clinical evaluation of collateral score in acute middle cerebral artery occlusion

Background/aim: Acute ischemic stroke (AIS) is characterized as a neurological deficit owing to an acute focal damage to the brain by cerebral infarction. A collateral score is the most significant factor evaluating the prognosis of AIS, its relationship with demographic data, serum biochemical parameters, and clinical disability in this field. Materials and methods: We conducted a single-center retrospective study with 100 patients with AIS within the first 6 h of ischemic stroke. Data for consecutive AIS patients were collected from February 2019 to May 2020. The collateral score was assessed by using developed scoring systems defined by Maas et al. The correlations between collateral score and demographic data, biochemical parameters, NIHSS scores (National Institutes of Health Stroke Scale), mRS (modified Rankin scale) scores were recorded. Results: The research was performed in 100 patients (median age, 71.55 ± 11.46 years), and there was a statistically significant difference between elevated erythrocyte distribution width (RDW) and Maas collateral score (insular cortex) (p = 0.024) and lymphocyte/ monocyte ratio (LMO) and Maas collateral (leptomeningeal) score (p = 0.025). Conclusion: In patients with acute MCA M1 occlusion, our analysis found a significant association between elevated RDW, low LMO parameters, and collateral score. We assume that, in terms of simple and quick usability in acute stroke prognosis, these parameters are useful and functional as a new biomarker.

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1. Sacco RL, Kasner SE, Broderick JP, Caplan LR, Connors JJ et al. An updated definition of stroke for the 21st century: a statement for healthcare professionals from the American Heart Association/ American Stroke Association. Stroke. 2013; 44(7): 2064-2089. doi: 10.1161/STR.0b013e318296aeca
2. Babür Dora, Sevin Balkan. Identification and comparison of etiologic subtypes in ischemic stroke according to the TOAST (Trial of Org 10172 in Acute Stroke) criteria. Turkish Journal of Cerebrovascular Diseases. 2001; 7(2): 35-39.
3. Bozzao L, Fantozzi LM, Bastianello S, Bozzao A, Fieschi C. Early collateral blood supply and late parenchymal brain damage in patients with middle cerebral artery occlusion. Stroke. 1989; 20(6): 735-740. doi: 10.1161/01.str.20.6.735
4. Brozici M, van der Zwan A, Hillen B. Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke 2003; 34: 2750– 2762.
5. Menon BK, Smith EE, Modi J, Patel SK, Bhatia R et al. American Journal of Neuroradiology. 2011; 32(9): 1640-1645. doi: https:// doi.org/10.3174/ajnr.A2564
6. Camargo EC, Furie KL, Singhal AB, Roccatagliata L, Cunnane ME et al. Acute brain infarct: detection and delineation with CT angiographic source images versus nonenhanced CT scans. Radiology. 2007; 244(2): 541-548. doi: 10.1148/radiol.2442061028
7. Aviv RI, Shelef I, Malam S, Chakraborty S, Sahlas DJ et al. Early stroke detection and extent: impact of experience and the role of computed tomography angiography source images. Clinical Radiology. 2007; 62(5): 447-452. doi: 10.1016/j. crad.2006.11.019
8. Hendrikse J, Hartkamp MJ, Hillen B, Mali WP, van der Grond J. Collateral ability of the circle of Willis in patients with unilateral internal carotid artery occlusion: border zone infarcts and clinical symptoms. Stroke. 2001; 32(12): 2768- 2773. doi: 10.1161/hs1201.099892
9. Liebeskind DS. Collateral circulation. Stroke. 2003; 34(9): 2279- 2284.
10. Liebeskind DS. Neuroprotection from the collateral perspective. IDrugs. 2005; 8(3): 222-228.
11. Shuaib A, Butcher K, Mohammad AA, Saqqur M, Liebeskind DS. Collateral blood vessels in acute ischaemic stroke: a potential therapeutic target. Lancet Neurology 2011; 10(10): 909-921. doi: 10.1016/S1474-4422(11)70195-8
12. Hendrikse J, van Raamt AF, van der Graaf Y, Mali WP, van der Grond J. Distribution of cerebral blood flow in the circle of Willis. Radiology. 2005; 235(1): 184-189. doi: 10.1148/ radiol.2351031799
13. Cuccione E, Padovano G, Versace A. Ferrarese C, Berette S. Cerebral collateral circulation in experimental ischemic stroke. Experimental & Translational Stroke Medicine. 2016; 8: 1-2.
14. Campbell BC, Christensen S, Tress BM, Churilov L, Desmond PM et al. Failure of collateral blood flow is associated with infarct growth in ischemic stroke. Journal of Cerebral Blood Flow Metabolism. 2013; 33(8): 1168-1172. doi: 10.1038/ jcbfm.2013.77
15. Zerna C, Thomalla G, Campbell BCV, Rha JH, Hill MD. Current practice and future directions in the diagnosis and acute treatment of ischaemic stroke. Lancet. 2018; 392(10154): 1247- 1256. doi: 10.1016/S0140-6736(18)31874-9
16. Kim SJ, Noh HJ, Yoon CW, Kim KH, Jeon PB· et al. Multiphasic perfusion computed tomography as a predictor of collateral flow in acute ischemic stroke: comparison with digital subtraction angiography. European Neurology. 2012; 67: 252– 255.
17. Boers AMM, Sales Barros R, Jansen IGH, Berkhemer OA, Beenen LFM et al. Value of Quantitative Collateral Scoring on CT Angiography in Patients with Acute Ischemic Stroke. American Journal of Neuroradiology. 2018; 39(6): 1074-1082. doi: 10.3174/ajnr.A5623
18. Tan IYL, Demchuk AM, Hopyan J, Zhang L, Gladstone D et al. CT angiography clot burden score and collateral score: correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. American Journal of Neuroradiology. 2009; 30(3): 525-531. doi: https://doi.org/10.3174/ajnr.A1408
19. Zhang X, Zhang M, Ding W, Yan S, Liebeskind DS et al. Distinct predictive role of collateral status on clinical outcome in variant stroke subtypes of acute large arterial occlusion. European Journal of Neuro.logy. 2018; 25(2): 293-300. doi: 10.1111/ ene.13493
20. Campbell BC, Mitchell PJ, Kleinig TJ et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. The New England Journal of Medicine. 2015; 372: 1009-1018. doi: 10.1056/NEJMoa1414792
21. Saposnik G, Strbian D. Enlightenment and challenges offered by DAWN trial (DWI or CTP Assessment With Clinical Mismatch in the Triage of Wake Up and Late Presenting Strokes Undergoing Neurointervention With Trevo. Stroke. 2018; 49: 498–500.
22. McVerry F, Liebeskind DS, Muir KW. Systematic review of methods for assessing leptomeningeal collateral flow. American Journal of Neuroradiology. 2012; 33(3): 576–582.
23. Maas MB, Lev MH, Ay H, Singhal AB, Greer DM et al. Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke. 2009; 40(9): 3001-3005. doi: 10.1161/ STROKEAHA.109.552513
24. Lima FO, Furie KL, Silva GS, Lev MH, Camargo EC et al. The pattern of leptomeningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke. 2010; 41(10): 2316-2322. doi: 10.1161/STROKEAHA.110.592303
25. Miteff F, Levi CR, Bateman GA, Spratt N, McElduff P et al. The independent predictive utility of computed tomography angiographic collateral status in acute ischaemic stroke. Brain. 2009; 132(8): 2231-2238. doi: 10.1093/brain/awp155
26. Mangiafico S, Consoli A, Renieri L, Rosi A, De Renzis A et al. Semi-quantitative and qualitative evaluation of pial leptomeningeal collateral circulation in acute ischemic stroke of the anterior circulation: the Careggi Collateral Score. Italian Journal of Anatomy and Embryology. 2013; 118(3): 277-287.
27. Yeo LL, Paliwal P, Teoh HL, Seet RC, Chan BP et al. Assessment of intracranial collaterals on CT angiography in anterior circulation acute ischemic stroke. American Journal of Neuroradiology. 2015; 36(2): 289-294.
28. Hossmann KA. Viability thresholds and the penumbra of focal ischemia. Annals of Neurology. 1994; 36: 557- 565.
29. Wong EH, Pullicino PM, Benedict R. Deep cerebral infarcts extending to the subinsular region. Stroke. 2001; 32: 2272- 2277.
30. Semba RD, Patel KV, Ferrucci L, Sun K, Roy CN et al. Serum antioxidants and inflammation predict red cell distribution width in older women: the Women’s Health and Aging Study. Clinical Nutrition. 2010; 29(5): 600-604. doi: 10.1016/j. clnu.2010.03.001
31. Cases N, Aguiló A, Tauler P, Sureda A, Lıompart I et al. Differential response of plasma and immune cell’s vitamin E levels to physical activity and antioxidant vitamin supplementation. European Journal of Clinical Nutrition. 2005; 59: 781–788.
32. Pascual-Figal DA, Bonaque JC, Redondo B, Caro C, ManzanoFernandez S et al. Red blood cell distribution width predicts long-term outcome regardless of anaemia status in acute heart failure patients. European Journal of Heart Failure. 2009; 11(9): 840-846. doi: 10.1093/eurjhf/hfp109
33. Al-Najjar Y, Goode KM, Zhang J, Cleland JG, Clark AL. Red cell distribution width: an inexpensive and powerful prognostic marker in heart failure. European Journal of Heart Failure. 2009; 11(12): 1155-1162.
34. Felker GM, Allen LA, Pocock SJ, Shaw LK, McMurray JJ et al. Red cell distribution width as a novel prognostic marker in heart failure: data from the CHARM Program and the Duke Databank. Journal of the American College of Cardiology. 2007; 50(1): 40-47. doi: 10.1016/j.jacc.2007.02.067
35. Dabbah S, Hammerman H, Markiewicz W, Aronson D. Relation between red cell distribution width and clinical outcomes after acute myocardial infarction. American Journal of Cardiology. 2010; 105(3): 312-317. doi: 10.1016/j.amjcard.2009.09.027
36. Ye Z, Smith C, Kullo IJ. Usefulness of red cell distribution width to predict mortality in patients with peripheral artery disease. American Journal of Cardiology. 2011; 107: 1241–1245.
37. Perlstein TS, Weuve J, Pfeffer MA, Beckman JA. Red blood cell distribution width and mortality risk in a community-based prospective cohort. Archieve of Internal Medicine. 2009; 169(6): 588-594.
38. Patel KV, Ferrucci L, Ershler WB, Longo DL, Guralnik JM. Red blood cell distribution width and the risk of death in middleaged and older adults. Archieve of Internal Medicine. 2009; 169(5): 515-523.
39. Kara H, Degirmenci S, Bayir A, Ak A., Akinci M et al. Red cell dis tribution width and neurological scoring systems in acute stroke patients. Neuropsychiatric Disease and Treatment. 2015; 11: 733–739.
40. Jia H, Li H, Zhang Y, Li C, Hu Y et al. Association between red blood cell distribution width (RDW) and carotid artery atherosclerosis (CAS) in patients with primary ischemic stroke. Archieve of Gerontology Geriatrics. 2015; 61(1): 72-75.
41. Turcato G, Cappellari M, Follador L, Dilda A, Bonora A et al. Red Blood Cell Distribution Width Is an Independent Predictor of Outcome in Patients Undergoing Thrombolysis for Ischemic Stroke. Seminars in thrombosis and hemostasis. 2017; 43(1): 30-35. doi: 10.1055/s-0036-1592165
42. Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nature Medicine. 2001; 7: 796–808.
43. Tokgöz S, Kayrak M, Akpinar Z, Seyithanoğlu A, Güney F et al. Neutrophil lymphocyte ratio as a predictor of stroke. Journal of Stroke and Cerebrovascular Diseases. 2013; 22(7): 1169-1174.
44. Zhu B, Pan Y, Jing J, Meng X, Zhao X et al. Neutrophil counts, neutrophil ratio, and new stroke in minor ischemic stroke or TIA. Neurology. 2018; 90(21): e1870-e1878.
45. Brooks SD, Spears C, Cummings C, VanGilder RL, Stinehart KR et al. Admission neutrophil-lymphocyte ratio predicts 90 day outcome after endovascular stroke therapy. Journal of Neurointervention Surgery. 2014; 6(8) : 578-583. doi: 10.1136/ neurintsurg-2013-01078
46. Lux D, Alakbarzade V, Bridge L, Clark CN, Clarke B et al. The association of neutrophil-lymphocyte ratio and lymphocytemonocyte ratio with 3-month clinical outcome after mechanical thrombectomy following stroke. Journal of Neuroinflammation. 2020;17(1): 60-64. doi: 10.1186/s12974- 020-01739-y
47. Semerano A, Laredo C, Zhao Y, Rudilosso S, Renú A et al. Leukocytes, Collateral Circulation, and Reperfusion in Ischemic Stroke Patients Treated With Mechanical Thrombectomy. Stroke. 2019 ; 50(12): 3456-3464. doi: 10.1161/ STROKEAHA.119.026743