Skip to main content

Advertisement

SpringerLink
Log in

Baseline severity and soluble vascular cell adhesion molecule 1 (sVCAM-1) as biomarker predictors of short-term mortality in acute ischemic stroke

  • Original Article
  • Published:
Metabolic Brain Disease Aims and scope Submit manuscript

Abstract

The aim was to investigate the association between plasma levels of cellular adhesion molecules (CAMs) and risk factors, subtypes, severity and short-term mortality of acute ischemic stroke (IS), and to identify a panel of biomarkers to predict short-term mortality after IS. The prospective study evaluated 132 IS patients within 24 h of their hospital admission. The baseline IS severity was assessed using the National Institutes Health Stroke Scale (NIHSS) and categorized as mild (NIHSS < 5), moderate (NIHSS 5–14) and severe (NIHSS ≥ 15). After three-month follow-up, the disability was assessed using the modified Rankin Scale (mRS); moreover, the patients were classified as survivors and non-survivors. Baseline inflammatory and anti-inflammatory cytokines and soluble CAMs were evaluated. Twenty-nine (21.9%) IS patients were non-survivors and showed higher NIHSS and soluble vascular cellular adhesion molecule 1 (sVCAM-1) than the survivors. The sVCAM-1 levels positively correlated with age, homocysteine, severity, and disability. The model #3 combining sVCAM-1 and NIHSS showed better results to predict short-term mortality with an area under the curve receiving operating characteristics (AUC/ROC) of 0.8841 [95% confidence interval (CI): 0.795–0.941] than the models with sVCAM-1 and NIHSS alone, with positive predictive value of 68.0%, negative predictive value of 91.3%, and accuracy of 86.5%. In conclusion, the combined model with baseline severity of IS and sVCAM-1 levels can early predict the prognosis of IS patients who may benefit with therapeutic measures of personalized therapy that taken into account these biomarkers. Moreover, this result suggests that VCAM-1 might be a potential target for the therapeutic strategies in IS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data and materials are available.

The protocol was approved by the Institutional Research Ethics Committees of University of Londrina, Paraná, Brazil (CAAE 61361416.9.0000.5231) and all of the individuals invited were informed in detail about the research and gave written Informed Consent.

References

  • Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL et al (1993) 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 24(1):35–41

    Article  Google Scholar 

  • Becker K, Kindrick D, Relton J, Harlan J, Winn R (2001) Antibody to the α4 integrin decreases infarct size in transient focal cerebral ischemia in rats. Stroke 32(1):206–211. https://doi.org/10.1161/01.str.32.1.206

    Article  CAS  Google Scholar 

  • Bitsch A, Klene W, Murtada L, Prange H, Rieckmann P (1998) A longitudinal prospective study of soluble adhesion molecules in acute stroke. Stroke 29(10):2129–2135. https://doi.org/10.1161/01.str.29.10.2129

    Article  CAS  Google Scholar 

  • Blann A, Kumar P, Krupinski J, McCollum C, Beevers DG, Lip GY (1999) Soluble intercellular adhesion molecule-1, E-selectin, vascular cell adhesion molecule-1 and von Willebrand factor in stroke. Blood Coagul Fibrinolysis 10(1):277–284. https://doi.org/10.1097/00001721-199907000-00009

    Article  CAS  Google Scholar 

  • Brazil (2013) Manual of routines for attention to stroke / Ministry of Health, Health Care Secretariat, Department of Specialized Care. - Brasília: Publisher of the Ministry of Health, p 50 

  • Brott T, Adams HP Jr, Olinger CP, Marler JR, Barsan WG, Biller J et al (1989) Measurements of acute cerebral infarction: a clinical examination scale. Stroke 20(7):864–870. https://doi.org/10.1161/01.str.20.7.864

    Article  CAS  Google Scholar 

  • Carluccio MA, Ancora MA, Massaro M, Carluccio M, Scoditti E, Diostante A et al (2007) Homocysteine induces VCAM-1 gene expression through NF-κB and NAD(P)H oxidase activation: protective role of Mediterranean diet polyphenolic antioxidants. Am J Physiol Heart Circ Physiol 293(4):H2344–H2354. https://doi.org/10.1152/ajpheart.00432.2007

    Article  CAS  Google Scholar 

  • Castillo J, Alvarez-Sabin J, Martínez-Vila E, Montaner J, Sobrino T, Vivancos J (2009) Inflammation markers and prediction of post-stroke vascular disease recurrence: the MITICO study. J Neurol 256(2):217–224. https://doi.org/10.1007/s00415-009

    Article  CAS  Google Scholar 

  • Cavusoglu Y, Timuralp B, Us T, Akgün Y, Kudaiberdieva G, Gorenek B, Unalir A et al (2004) Cigarette smoking increases plasma concentrations of vascular cell adhesion molecule-1 in patients with coronary artery disease. Angiology 55(4):397–402. https://doi.org/10.1177/000331970405500406

  • Chen L, Wang W, Zhang S, Liu H, Yuan X, Yang X et al (2021) Value of Barthel, PLAN and NIHSS scores for predicting the death of patients with acute ischemic stroke during their 5-year follow-up. J Clin Neurosci 90:94–98. https://doi.org/10.1016/j.jocn.2021.05.049

    Article  Google Scholar 

  • Cook-Mills JM, Marchese ME, Abdala-Valencia H (2011) Vascular cell adhesion molecule-1 expression and signaling during disease: regulation by reactive oxygen species and antioxidants. Antioxid Redox Signal 15(6):1607–1638. https://doi.org/10.1089/ars.2010.3522

    Article  CAS  Google Scholar 

  • de Lemos JA, Hennekens CH, Ridker PM (2000) Plasma concentration of soluble vascular cell adhesion molecule-1 and subsequent cardiovascular risk. J Am Coll Cardiol 36(2):423–426. https://doi.org/10.1016/S0735-1097(00)00742-7

    Article  Google Scholar 

  • Draznin B, Aroda VR, Bakris G, Benson G, Brown FM, Freeman R et al (2022) 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2022. Diabetes Care 45(Supplement 1):S17–S38

    Google Scholar 

  • Elkind MS, Veltkamp R, Montaner J, Johnston SC, Singhal AB, Becker K et al (2020) Natalizumab in acute ischemic stroke (ACTION II): a randomized, placebo-controlled trial. Neurology 95(8):e1091–e1104. https://doi.org/10.1212/WNL.0000000000010038

    Article  CAS  Google Scholar 

  • Elkins J, Veltkamp R, Montaner J, Johnston SC, Singhal AB, Becker K et al (2017) Safety and efficacy of natalizumab in patients with acute ischaemic stroke (ACTION): a randomised, placebo-controlled, double-blind phase 2 trial. Lancet Neurol 16(3):217–226. https://doi.org/10.1016/S1474-4422(16)30357-X

    Article  CAS  Google Scholar 

  • Fassbender K, Mössner R, Motsch L, Kischka U, Grau A, Hennerici M (1995) Circulating selectin-and immunoglobulin-type adhesion molecules in acute ischemic stroke. Stroke 26(8):1361–1364. https://doi.org/10.1161/01.str.26.8.1361

    Article  CAS  Google Scholar 

  • Feigin VL, Stark BA, Johnson CO, Roth GA, Bisignano C, Abady GG et al (2021) Global, regional, and national burden of stroke and its risk factors, 1990–2019: A systematic analysis for the Global Burden of Disease Study 2019. Lancet Neurol 20(10):795–820. https://doi.org/10.1016/S1474-4422(21)00252-0

    Article  CAS  Google Scholar 

  • Frijns CJ, Kappelle LJ (2002) Inflammatory cell adhesion molecules in ischemic cerebrovascular disease. Stroke 33:2115–2122. https://doi.org/10.1161/01.str.0000021902.33129.69

    Article  CAS  Google Scholar 

  • Frijns CJM, Kappelle LJ, Gijn JV, Nieuwenhuis HK, Sixma JJ, Fijnheer R (1997) Soluble adhesion molecules reflect endothelial cell activation in ischemic stroke and in carotid atherosclerosis. Stroke 28(11):2214–2218. https://doi.org/10.1161/01.str.28.11.2214

    Article  CAS  Google Scholar 

  • Gagliardi RJ, André C, Fukujima MM, Melo-Souza SE, Zétola VF (2005) Abordagem da doença carotídea na fase aguda do acidente vascular cerebral: opinião nacional. Arq Neuropsiquiatr 63:709–712. https://doi.org/10.1590/s0004-282x2005000400032

    Article  Google Scholar 

  • Ghaisas NK, Shahi CN, Foley B, Goggins M, Crean P, Kelly A et al (1997) Elevated levels of circulating soluble adhesion molecules in peripheral blood of patients with unstable angina. Am J Cardiol 80(5):617–619. https://doi.org/10.1016/S0002-9149(97)00432-3

    Article  CAS  Google Scholar 

  • Hasan N, McColgan P, Bentley P, Edwards RJ, Sharma P (2012) Towards the identification of blood biomarkers for acute stroke in humans: a comprehensive systematic review. British J Clin Pharmacol 74(2):230–240. https://doi.org/10.1111/j.1365-2125.2012.04212.x

    Article  CAS  Google Scholar 

  • Hayek A, Paccalet A, Mechtouff L, Da Silva CC, Ivanes F, Falque H et al (2021) Kinetics and prognostic value of soluble VCAM-1 in ST-segment elevation myocardial infarction patients. Immun Inflamm Dis 9(2):493–501. https://doi.org/10.1002/iid3.409

    Article  CAS  Google Scholar 

  • James PA, Oparil S, Carter BL, Cushman WC, Dennison-Himmelfarb C, Handler J et al (2014) 2014 Evidence-based guideline for the management of high blood pressure in adults: report from the panel members appointed to the Eighth Joint National Committee (JNC 8). JAMA 311(5):507–520

    Article  CAS  Google Scholar 

  • Krieglstein CF, Granger DN (2001) Adhesion molecules and their role in vascular disease. Am J Hypertens 14(S3):44S-54S. https://doi.org/10.1016/s0895-7061(01)02069-6

    Article  CAS  Google Scholar 

  • KusvuranOzkan A, Umit Yemisci O, NurSaracgilCosar S, Oztop P, Turhan N (2013) Can high-sensitivity C-reactive protein and ferritin predict functional outcome in acute ischemic stroke? A Prospective Study. Top Stroke Rehabil 20(6):528–536. https://doi.org/10.1310/tsr2006-528

    Article  Google Scholar 

  • Lehmann MF, Kallaur AP, Oliveira SR, Alfieri DF, Delongui F, de Sousa PJ et al (2015) Inflammatory and metabolic markers and short-time outcome in patients with acute ischemic stroke in relation to TOAST subtypes. Met Brain Dis 30(6):1417–1428. https://doi.org/10.1007/s11011-015-9731-8

    Article  CAS  Google Scholar 

  • Lehmann ALCF, Alfieri DF, de Araújo MCM, Trevisani ER, Nagao MR, Pesente FS et al (2021) Carotid intima media thickness measurements coupled with stroke severity strongly predict short-term outcome in patients with acute ischemic stroke: A machine learning study. Met Brain Dis 36(7):1747–1761. https://doi.org/10.1007/s11011-021-00784-7

    Article  Google Scholar 

  • Lehmann ALCF, Alfieri DF, de Araújo MCM, Trevisani ER, Nagao MR, Pesente FS et al (2022) Immune-inflammatory, coagulation, adhesion, and imaging biomarkers combined in machine learning models improve the prediction of death 1 year after ischemic stroke. Clin Exp Med 22(1):111–123. https://doi.org/10.1007/s10238-021-00732-w

    Article  CAS  Google Scholar 

  • Licata G, Tuttolomondo A, Di Raimondo D, Corrao S, Di Sciacca R, Pinto A (2009) Immuno-inflammatory activation in acute cardio-embolic strokes in comparison with other subtypes of ischaemic stroke. Thromb Haemostasis 101(05):929–937

    Article  CAS  Google Scholar 

  • Lin CC, Pan CS, Wang CY, Liu SW, Hsiao LD, Yang CM (2015) Tumor necrosis factor-alpha induces VCAM-1-mediated inflammation via c-Src-dependent transactivation of EGF receptors in human cardiac fibroblasts. J Biomed Sci 22(1):1–15. https://doi.org/10.1186/s12929-015-0165-8

    Article  CAS  Google Scholar 

  • Llovera G, Hofmann K, Roth S, Salas-Pérdomo A, Ferrer-Ferrer M, Perego C et al (2015) Results of a preclinical randomized controlled multicenter trial (pRCT): Anti-CD49d treatment for acute brain ischemia. Sci Transl Med 7(299):299ra121-299ra121. https://doi.org/10.1126/scitranslmed.aaa9853

    Article  CAS  Google Scholar 

  • Ma Q, Chen S, Klebe D, Zhang JH, Tang J (2013) Adhesion molecules in CNS disorders: biomarker and therapeutic targets. CNS Neurol Disord Drug Targets 12(3):392–404. https://doi.org/10.2174/1871527311312030012

    Article  CAS  Google Scholar 

  • Maes M, Carvalho AF (2018) The Compensatory Immune-Regulatory Reflex System (CIRS) in Depression and Bipolar Disorder. Mol Neurobiol 55:8885–8903. https://doi.org/10.1007/s12035-018-1016-x

    Article  CAS  Google Scholar 

  • Maes M, Nikiforov NG, Plaimas K, Suratanee A, Alfieri DF, VissociReiche EM (2021) New drug targets to prevent death due to stroke: a review based on results of protein-protein interaction network, enrichment, and annotation analyses. Int J Mol Sci 22(22):12108. https://doi.org/10.3390/ijms222212108

    Article  CAS  Google Scholar 

  • Marta-Enguita J, Navarro-Oviedo M, Rubio-Baines I, Aymerich N, Herrera M, Zandio B et al (2021) Association of calprotectin with other inflammatory parameters in the prediction of mortality for ischemic stroke. J Neuroinflammation 18(1):1–13. https://doi.org/10.1186/s12974-020-02047-1

    Article  CAS  Google Scholar 

  • Martins SCO, Freitas GRD, Pontes-Neto OM, Pieri A, Moro CHC, Jesus PAPD et al (2012) Guidelines for acute ischemic stroke treatment: part II: stroke treatment. Arq Neuropsiquiatr 70:885–893. https://doi.org/10.1590/s0004-282x2012001100012

    Article  Google Scholar 

  • Miles EA, Thies F, Wallace FA, Powell JR, Hurst TL, Newsholme EA et al (2001) Influence of age and dietary fish oil on plasma soluble adhesion molecule concentrations. Clin Sci 100(1):91–100

    Article  CAS  Google Scholar 

  • Morisaki N (1997) New indices of ischemic heart disease and aging: studies on the serum levels of soluble intercellular adhesion molecule-1 (ICAM-1) and soluble vascular cell adhesion molecule-1 (VCAM-1) in patients with hypercholesterolemia and ischemic heart disease. Atherosclerosis 131(1):43–48. https://doi.org/10.1016/s0021-9150(97)06083-8

    Article  CAS  Google Scholar 

  • Mulvihill NT, Foley JB, Murphy RT, Curtin R, Crean PA, Walsh M (2001) Risk stratification in unstable angina and non-Q wave myocardial infarction using soluble cell adhesion molecules. Heart 85(6):623–627. https://doi.org/10.1136/heart.85.6.623

    Article  CAS  Google Scholar 

  • Nash MC, Wade AM, Shah V, Dillon MJ (1996) Normal levels of soluble E-selectin, soluble intercellular adhesion molecule-1 (sICAM-1), and soluble vascular cell adhesion molecule-1 (sVCAM-1) decrease with age. Clin Exp Immunol 103(1):167–170. https://doi.org/10.1046/j.1365-2249.1996.925616.x

    Article  CAS  Google Scholar 

  • Oliveira-Filho J, Martins SCO, Pontes-Neto OM, Longo A, Evaristo EF, Carvalho JJFD et al (2012) Guidelines for acute ischemic stroke treatment: part I. Arq Neuropsiquiatr 70(8):621–629. https://doi.org/10.1590/s0004-282x2012000800012

    Article  Google Scholar 

  • Park KY, Chung PW, Kim YB, Moon HS, Suh BC, Won YS et al (2015) Serum vitamin D status as a predictor of prognosis in patients with acute ischemic stroke. Cerebrovasc Dis 40:73–80

    Article  CAS  Google Scholar 

  • Patel RB, Colangelo LA, Bielinski SJ, Larson NB, Ding J, Allen NB et al (2020) Circulating vascular cell adhesion molecule-1 and incident heart failure: the multi-ethnic study of atherosclerosis (MESA). J Am Heart Assoc 9(22):e019390. https://doi.org/10.1161/JAHA.120.019390

    Article  Google Scholar 

  • Pawluk H, Woźniak A, Grześk G, Kołodziejska R, Kozakiewicz M, Kopkowska E et al (2020) The role of selected pro-inflammatory cytokines in pathogenesis of ischemic stroke. Clin Interv Aging 15:469–484. https://doi.org/10.2147/CIA.S233909

    Article  CAS  Google Scholar 

  • Powers WJ (2020) Acute ischemic stroke. N Engl J Med 383(3):252–260. https://doi.org/10.1056/NEJMcp1917030

    Article  Google Scholar 

  • Puig N, Jiménez-Xarrié E, Camps-Renom P, Benitez S (2020) Search for reliable circulating biomarkers to predict carotid plaque vulnerability. Int J Mol Sci 21(21):8236. https://doi.org/10.3390/ijms21218236

  • Purschwitz K, Rassoul F, Reuter W, Purschwitz R, Jahn N, Kellert D et al (2001) Soluble leukocyte adhesion molecules in vegetarians of various ages. Z Gerontol Geriatr 34(6):476–479. https://doi.org/10.1007/s003910170022

  • Rallidis LS, Zolindaki MG, Vikelis M, Kaliva K, Papadopoulos C, Kremastinos DT (2009) Elevated soluble intercellular adhesion molecule-1 levels are associated with poor short-term prognosis in middle-aged patients with acute ischemic stroke. Int J Cardiol 132(2):216–220. https://doi.org/10.1016/j.ijcard.2007.11.031

  • Ramiro L, Simats A, García-Berrocoso T, Montaner J (2018) Inflammatory molecules might become both biomarkers and therapeutic targets for stroke management. Ther Adv Neurol Disord 11:1–24. https://doi.org/10.1177/1756286418789340

    Article  CAS  Google Scholar 

  • R Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/

  • Reiche EMV, Gelinksi JR, Alfieri DF, Flauzino T, Lehmann MF, de Araújo MCM et al (2019) Immune-inflammatory, oxidative stress and biochemical biomarkers predict short-term acute ischemic stroke death. Met Brain Dis 34(3):789–804. https://doi.org/10.1007/s11011-019-00403-6

    Article  CAS  Google Scholar 

  • Richard S, Lagerstedt L, Burkhard PR, Debouverie M, Turck N, Sanchez JC (2015) E-selectin and vascular cell adhesion molecule-1 as biomarkers of 3-month outcome in cerebrovascular diseases. J Inflamm 12:61. https://doi.org/10.1186/s12950-015-0106-z

    Article  CAS  Google Scholar 

  • Saber H, Saver JL (2020) Distributional validity and prognostic power of the national institutes of health stroke scale in US administrative claims data. JAMA Neurol 77(5):606–612. https://doi.org/10.1001/jamaneurol.2019.5061

    Article  Google Scholar 

  • Silverman MD, Tumuluri RJ, Davis M, Lopez G, Rosenbaum JT, Lelkes PI (2002) Homocysteine upregulates vascular cell adhesion molecule-1 expression in cultured human aortic endothelial cells and enhances monocyte adhesion. Arterioscler Thromb Vasc Biol 22(4):587–592

    Article  CAS  Google Scholar 

  • Simundic AM, Basic V, Demarin V, Vrkic N, Kunovic B, Stefanovic M et al (2004) Soluble adhesion molecules in acute ischemic stroke. Clin Invest Med 27(2):86–93

    CAS  Google Scholar 

  • Singh RJ, Mason JC, Lidington EA, Edwards DR, Nuttall RK, Khokha R et al (2005) Cytokine stimulated vascular cell adhesion molecule-1 (VCAM-1) ectodomain release is regulated by TIMP-3. Cardiovasc Res 67(1):39–49

    Article  CAS  Google Scholar 

  • Supanc V, Biloglav Z, Kes VB, Demarin V (2011) Role of cell adhesion molecules in acute ischemic stroke. Ann Saudi Med 31(4):365–370

    Article  Google Scholar 

  • The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) (2002) Third report of the national cholesterol education program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III) final report. Circulation 106(25):3143–3421

    Article  Google Scholar 

  • Tuttolomondo A, Di Sciacca R, Di Raimondo D, Serio A, D’Aguanno G, La Placa S et al (2009) Plasma levels of inflammatory and thrombotic/fibrinolytic markers in acute ischemic strokes: relationship with TOAST subtype, outcome and infarct site. J Neuroimmunology 215(1–2):84–89

    Article  CAS  Google Scholar 

  • Vemuganti R, Dempsey RJ, Bowen KK (2004) Inhibition of intercellular adhesion molecule-1 protein expression by antisense oligonucleotides is neuroprotective after transient middle cerebral artery occlusion in rat. Stroke 35(1):179–184. https://doi.org/10.1161/01.STR.0000106479.53235.3E

    Article  CAS  Google Scholar 

  • Wang X, Feuerstein GZ (1995) Induced expression of adhesion molecules following focal brain ischemia. J Neurotrauma 12(5):825–832. https://doi.org/10.1089/neu.1995.12.825

    Article  CAS  Google Scholar 

  • Wang Y, Ji H, Tong Y, Zhang Z (2014) Prognostic value of serum 25-hydroxyvitamin D in patients with stroke. Neurochem Res 39:1332–1337

    Article  CAS  Google Scholar 

  • Yang C, Hawkins KE, Candelario-Jalil DS, E (2019) Neuroinflammatory mechanisms of blood-brain barrier damage in ischemic stroke. Am J Physiol-Cell Physiol 316(2):C135–C153. https://doi.org/10.1152/ajpcell.00136.2018

  • Yilmaz G, Granger DN (2008) Cell adhesion molecules and ischemic stroke. Neurol Res 30(8):783–793. https://doi.org/10.1179/174313208X341085

  • Zaremba J, Losy J (2002) Adhesion molecules of immunoglobulin gene superfamily in stroke. Folia Morphol 61(1):1–6

    Google Scholar 

  • Zhao XJ, Li QX, Liu TJ, Wang DL, An YC, Zhang J et al (2018) Predictive values of CSS and NIHSS in the prognosis of patients with acute cerebral infarction: a comparative analysis. Medicine 97(39):e12419. https://doi.org/10.1097/MD.0000000000012419

    Article  Google Scholar 

  • Zou Y, Jung KJ, Kim JW, Yu BP, Chung HY (2004) Alteration of soluble adhesion molecules during aging and their modulation by calorie restriction. FASEB J 18(2):320–322. https://doi.org/10.1096/fj.03-0849fje

Download references

Acknowledgements

Thanks to the Institutional Program for Scientific Initiation Scholarship (PIBIC) of the National Council for Scientific and Technological Development (CNPq); Coordination for the Improvement of Higher Level of Education Personnel (CAPES) of Brazilian Ministry of Education: Finance Code 001; Araucaria Foundation, Paraná State, Brazil, Conv. 001/2017, Call nº 09/2016, Protocol 47.396; Clinical and Laboratory Pathophysiology Postgraduate Program, Health Sciences Center, State University of Londrina, Londrina, Paraná, Brazil.

Funding

The study was supported by grants from Fundação Araucária, Paraná State, Brazil, Conv. 001/2017, Call nº 09/2016, Protocol 47.396—Institutional Program of Basic and Applied Research; grants from Coordination for the Improvement of Higher Level of Education Personnel (CAPES) of Brazilian Ministry of Education: Finance Code 001; Institutional Program for Scientific Initiation Scholarship (PIBIC) of the National Council for Scientific and Technological Development (CNPq) of Brazil.

Author information

Authors and Affiliations

  1. Clinical and Laboratory Pathophysiology Postgraduate Program, Health Sciences Center, State University of Londrina, Paraná, Brazil

    Maria Caroline Martins de Araújo

  2. Department of Pharmaceutical Sciences, Health Sciences Center, State University of Londrina, Paraná, Brazil

    Daniela Frizon Alfieri

  3. Department of Clinical Medicine, Health Science Center and Radiology Service of the University Hospital, State University of Londrina, Paraná, Brazil

    Ana Lucia Cruz Fürstenberger Lehmann

  4. Laboratory of Research in Applied Immunology, Health Sciences Center, State University of Londrina, Paraná, Brazil

    Tamires Flauzino Luz, Emmanuelle Roberto Trevisani, Maisa Rocha Nagao, Leonardo Bodner de Freitas, Andrea Name Colado Simão & Edna Maria Vissoci Reiche

  5. Department of Pathology, Clinical Analysis, and Toxicology, Health Sciences Center, State University of Londrina, Av. Robert Koch, 60, Londrina, Paraná, CEP 86.038-440, Brazil

    Andrea Name Colado Simão & Edna Maria Vissoci Reiche

Authors
  1. Maria Caroline Martins de Araújo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniela Frizon Alfieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Lucia Cruz Fürstenberger Lehmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tamires Flauzino Luz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Emmanuelle Roberto Trevisani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maisa Rocha Nagao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Leonardo Bodner de Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andrea Name Colado Simão
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Edna Maria Vissoci Reiche
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

1) conception and design of the study: EMVR, ANCS; 2) acquisition of data: MCMA, DFA, ALFCL, ERT, MRN, LBF, TF, 3) statistical analysis: DFA; 4) analysis and interpretation of data: MCMA, DFA, EMVR; 5) drafting of the manuscript, tables and figures: MCMA, DFA, EMVR 6) manuscript review: EMVR.

Corresponding author

Correspondence to Edna Maria Vissoci Reiche.

Ethics declarations

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Consent for publication

The studied participants were informed about the present research, and a written consent form was taken from all of them before their enrollment. Moreover, all the authors and co-authors participated and contributed sufficiently in the research, and all of them concur with the submission. The manuscript has been approved by the responsible authorities where the work was carried out. The authors also concur that, if accepted, the manuscript shall not be published elsewhere in the same form in either the same or any other language, without the consent of the Editor-in Chief of Metabolic Brain Disease.

Conflict of interest

There is no conflict of interest to declare. None of the authors are involved in the publication process or have a financial or other beneficial interest in the products or concepts mentioned in the submitted manuscript.

Human rights

All procedures performed in this study involving human participants were in accordance with the ethical standards of the Institution and/or National Research Committee and with the World Medical Association 1964 Helsinki Declaration.

Standards for reporting

The manuscript was prepared taken into account the recommendations of the guidelines hosted by the Strengthening the Reporting of Observational studies in Epidemiology (STROBE). STROBE is used for observational studies (cohort, case–control, or cross-sectional designs) according to the STROBE statement (www.strobe-statement.org).

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Araújo, M.C.M., Alfieri, D.F., Lehmann, A.L.C.F. et al. Baseline severity and soluble vascular cell adhesion molecule 1 (sVCAM-1) as biomarker predictors of short-term mortality in acute ischemic stroke. Metab Brain Dis 38, 657–670 (2023). https://doi.org/10.1007/s11011-022-01116-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11011-022-01116-z

Keywords

Search

Navigation