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Relationship between thrombus attenuation and different stroke subtypes

  • Diagnostic Neuroradiology
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Abstract

Introduction

More insights in the etiopathogenesis of thrombi could be helpful in the treatment of patients with acute ischemic stroke. The aim of our study was to determine the relationship between presence of a hyperdense vessel sign and thrombus density with different stroke subtypes.

Methods

We included 123 patients with acute ischemic anterior circulation stroke and a visible occlusion on CT-angiography caused by cardioembolism (n = 53), large artery atherosclerosis (n = 55), or dissection (n = 15). Presence or absence of a hyperdense vessel sign was assessed and thrombus density was measured in Hounsfield Units (HU) on non-contrast 1 mm thin slices CT. Subsequently, occurrence of hyperdense vessel sign and thrombus density (absolute HU and rHU (=HU thrombus/HU contralateral)) were related with stroke subtypes.

Results

The presence of hyperdense vessel signs differed significantly among subtypes and was found in 45, 64 and 93 % of patients with cardioembolism, large artery atherosclerosis and dissection, respectively (p = 0.003). The mean HU and rHU (+95 % CI) of the thrombi in all vessels were respectively 56.1 (53.2–59.0) and 1.39 (1.33–1.45) in cardioembolism, 64.6 (62.2–66.9) and 1.59 (1.54–1.64) in large artery atherosclerosis and 76.4 (73.0–79.8) and 1.88 (1.79–1.97) in dissection (p < 0.0001). We found the same significant ranking order in the density of thrombi with hyperdense vessel signs (mean HU and rHU (+95 % CI), respectively): cardioembolism 61.3 (57.4–65.3) and 1.49 (57.4–65.3); large artery atherosclerosis 67.3 (64.9–69.7) and 1.65 (1.58–1.71); dissection 76.4 (72.6–80.1) and 1.89 (1.79–1.99, p < 0.0001).

Conclusion

Presence of a hyperdense vessel sign and thrombus density are related to stroke subtype.

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References

  1. Carod-Artal FJ, Egido JA (2009) Quality of life after stroke: the importance of a good recovery. Cerebrovasc Dis 27(Suppl 1):204–214

    Article  PubMed  Google Scholar 

  2. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, Moy CS, Mozaffarian D, Mussolino ME, Nichol G, Paynter NP, Soliman EZ, Sorlie PD, Sotoodehnia N, Turan TN, Virani SS, Wong ND, Woo D, Turner MB (2012) Heart disease and stroke statistics—2012 update: a report from the American Heart Association. Circulation 125:e2–e220

    Article  PubMed  Google Scholar 

  3. Williams GR, Jiang JG, Matchar DB, Samsa GP (1999) Incidence and occurrence of total (first-ever and recurrent) stroke. Stroke 30:2523–2528

    Article  PubMed  CAS  Google Scholar 

  4. Bejot Y, Caillier M, Ben Salem D, Couvreur G, Rouaud O, Osseby GV, Durier J, Marie C, Moreau T, Giroud M (2008) Ischaemic stroke subtypes and associated risk factors: a French population based study. J Neurol Neurosurg Psychiatry 79:1344–1348

    Article  PubMed  CAS  Google Scholar 

  5. Schulz UG, Rothwell PM (2003) Differences in vascular risk factors between etiological subtypes of ischemic stroke: importance of population-based studies. Stroke 34:2050–2059

    Article  PubMed  CAS  Google Scholar 

  6. Kolominsky-Rabas PL, Weber M, Gefeller O, Neundoerfer B, Heuschmann PU (2001) Epidemiology of ischemic stroke subtypes according to TOAST criteria: incidence, recurrence, and long-term survival in ischemic stroke subtypes: a population-based study. Stroke 32:2735–2740

    Article  PubMed  CAS  Google Scholar 

  7. Putaala J, Metso AJ, Metso TM, Konkola N, Kraemer Y, Haapaniemi E, Kaste M, Tatlisumak T (2009) Analysis of 1008 consecutive patients aged 15 to 49 with first-ever ischemic stroke: the Helsinki young stroke registry. Stroke 40:1195–1203

    Article  PubMed  Google Scholar 

  8. Mazighi M, Serfaty JM, Labreuche J, Laissy JP, Meseguer E, Lavallee PC, Cabrejo L, Slaoui T, Guidoux C, Lapergue B, Klein IF, Olivot JM, Abboud H, Simon O, Niclot P, Nifle C, Touboul PJ, Raphaeli G, Gohin C, Claeys ES, Amarenco P (2009) Comparison of intravenous alteplase with a combined intravenous-endovascular approach in patients with stroke and confirmed arterial occlusion (RECANALISE study): a prospective cohort study. Lancet Neurol 8:802–809

    Article  PubMed  CAS  Google Scholar 

  9. Caplan LR (2006) Antiplatelet therapy in stroke prevention: present and future. Cerebrovasc Dis 21(Suppl 1):1–6

    Article  PubMed  CAS  Google Scholar 

  10. Jang IK, Gold HK, Ziskind AA, Fallon JT, Holt RE, Leinbach RC, May JW, Collen D (1989) Differential sensitivity of erythrocyte-rich and platelet-rich arterial thrombi to lysis with recombinant tissue-type plasminogen activator. A possible explanation for resistance to coronary thrombolysis. Circulation 79:920–928

    Article  PubMed  CAS  Google Scholar 

  11. Zivin JA, Fisher M, DeGirolami U, Hemenway CC, Stashak JA (1985) Tissue plasminogen activator reduces neurological damage after cerebral embolism. Science 230:1289–1292

    Article  PubMed  CAS  Google Scholar 

  12. Niessen F, Hilger T, Hoehn M, Hossmann KA (2003) Differences in clot preparation determine outcome of recombinant tissue plasminogen activator treatment in experimental thromboembolic stroke. Stroke 34:2019–2024

    Article  PubMed  CAS  Google Scholar 

  13. Molina CA, Montaner J, Arenillas JF, Ribo M, Rubiera M, Alvarez-Sabin J (2004) Differential pattern of tissue plasminogen activator-induced proximal middle cerebral artery recanalization among stroke subtypes. Stroke 35:486–490

    Article  PubMed  Google Scholar 

  14. Cho KH, Lee DH, Kwon SU, Choi CG, Kim SJ, Suh DC, Kim JS, Kang DW (2012) Factors and outcomes associated with recanalization timing after thrombolysis. Cerebrovasc Dis 33:255–261

    Article  PubMed  CAS  Google Scholar 

  15. Puig J, Pedraza S, Demchuk A, Daunis IEJ, Termes H, Blasco G, Soria G, Boada I, Remollo S, Banos J, Serena J, Castellanos M (2012) Quantification of thrombus hounsfield units on noncontrast CT predicts stroke subtype and early recanalization after intravenous recombinant tissue plasminogen activator. AJNR Am J Neuroradiol 33:90–96

    Article  PubMed  CAS  Google Scholar 

  16. Wohner N (2008) Role of cellular elements in thrombus formation and dissolution. Cardiovasc Hematol Agents Med chem 6:224–228

    Article  PubMed  CAS  Google Scholar 

  17. Kirchhof K, Welzel T, Mecke C, Zoubaa S, Sartor K (2003) Differentiation of white, mixed, and red thrombi: value of CT in estimation of the prognosis of thrombolysis phantom study. Radiology 228:126–130

    Article  PubMed  Google Scholar 

  18. Kim EY, Heo JH, Lee SK, Kim DJ, Suh SH, Kim J, Kim DI (2006) Prediction of thrombolytic efficacy in acute ischemic stroke using thin-section noncontrast CT. Neurology 67:1846–1848

    Article  PubMed  CAS  Google Scholar 

  19. New PF, Aronow S (1976) Attenuation measurements of whole blood and blood fractions in computed tomography. Radiology 121:635–640

    PubMed  CAS  Google Scholar 

  20. Liebeskind DS, Sanossian N, Yong WH, Starkman S, Tsang MP, Moya AL, Zheng DD, Abolian AM, Kim D, Ali LK, Shah SH, Towfighi A, Ovbiagele B, Kidwell CS, Tateshima S, Jahan R, Duckwiler GR, Vinuela F, Salamon N, Villablanca JP, Vinters HV, Marder VJ, Saver JL (2011) CT and MRI early vessel signs reflect clot composition in acute stroke. Stroke 42:1237–1243

    Article  PubMed  Google Scholar 

  21. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 3rd (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 24:35–41

    Article  PubMed  Google Scholar 

  22. Kim YK, Schulman S (2009) Cervical artery dissection: pathology, epidemiology and management. Thromb Res 123:810–821

    Article  PubMed  CAS  Google Scholar 

  23. Chen CJ, Tseng YC, Lee TH, Hsu HL, See LC (2004) Multisection CT angiography compared with catheter angiography in diagnosing vertebral artery dissection. AJNR Am J Neuroradiol 25:769–774

    PubMed  Google Scholar 

  24. Leys D, Pruvo JP, Godefroy O, Rondepierre P, Leclerc X (1992) Prevalence and significance of hyperdense middle cerebral artery in acute stroke. Stroke 23:317–324

    Article  PubMed  CAS  Google Scholar 

  25. Rauch RA, Bazan C 3rd, Larsson EM, Jinkins JR (1993) Hyperdense middle cerebral arteries identified on CT as a false sign of vascular occlusion. AJNR Am J Neuroradiol 14:669–673

    PubMed  CAS  Google Scholar 

  26. Barber PA, Demchuk AM, Hudon ME, Pexman JH, Hill MD, Buchan AM (2001) Hyperdense sylvian fissure MCA "dot" sign: a CT marker of acute ischemia. Stroke 32:84–88

    Article  PubMed  CAS  Google Scholar 

  27. Bastianello S, Pierallini A, Colonnese C, Brughitta G, Angeloni U, Antonelli M, Fantozzi LM, Fieschi C, Bozzao L (1991) Hyperdense middle cerebral artery CT sign. Comparison with angiography in the acute phase of ischemic supratentorial infarction. Neuroradiology 33:207–211

    Article  PubMed  CAS  Google Scholar 

  28. Moulin T, Tatu L, Vuillier F, Cattin F (1999) Brain CT scan for acute cerebral infarction: early signs of ischemia. Rev Neurol 155:649–655

    PubMed  CAS  Google Scholar 

  29. Chaves CJ, Caplan LR (2000) Heparin and oral anticoagulants in the treatment of brain ischemia. J Neurol Sci 173:3–9

    Article  PubMed  CAS  Google Scholar 

  30. Vila A, Korytowski W, Girotti AW (2002) Spontaneous transfer of phospholipid and cholesterol hydroperoxides between cell membranes and low-density lipoprotein: assessment of reaction kinetics and prooxidant effects. Biochemistry 41:13705–13716

    Article  PubMed  CAS  Google Scholar 

  31. Kockx MM, Cromheeke KM, Knaapen MW, Bosmans JM, De Meyer GR, Herman AG, Bult H (2003) Phagocytosis and macrophage activation associated with hemorrhagic microvessels in human atherosclerosis. Arterioscler Thromb Vasc Biol 23:440–446

    Article  PubMed  CAS  Google Scholar 

  32. Kolodgie FD, Gold HK, Burke AP, Fowler DR, Kruth HS, Weber DK, Farb A, Guerrero LJ, Hayase M, Kutys R, Narula J, Finn AV, Virmani R (2003) Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 349:2316–2325

    Article  PubMed  CAS  Google Scholar 

  33. Takaya N, Yuan C, Chu B, Saam T, Polissar NL, Jarvik GP, Isaac C, McDonough J, Natiello C, Small R, Ferguson MS, Hatsukami TS (2005) Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Circulation 111:2768–2775

    Article  PubMed  Google Scholar 

  34. Rao DS, Goldin JG, Fishbein MC (2005) Determinants of plaque instability in atherosclerotic vascular disease. Cardiovasc Pathol Off J Soc Cardiovasc Pathol 14:285–293

    Article  Google Scholar 

  35. Virmani R, Kolodgie FD, Burke AP, Finn AV, Gold HK, Tulenko TN, Wrenn SP, Narula J (2005) Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol 25:2054–2061

    Article  PubMed  CAS  Google Scholar 

  36. Redgrave JN, Lovett JK, Gallagher PJ, Rothwell PM (2006) Histological assessment of 526 symptomatic carotid plaques in relation to the nature and timing of ischemic symptoms: the Oxford plaque study. Circulation 113:2320–2328

    Article  PubMed  CAS  Google Scholar 

  37. Wysokinski WE, Owen WG, Fass DN, Patrzalek DD, Murphy L, McBane RD 2nd (2004) Atrial fibrillation and thrombosis: immunohistochemical differences between in situ and embolized thrombi. J thromb haemost JTH 2:1637–1644

    Article  CAS  Google Scholar 

  38. Mohan IV (2013) Current optimal assessment and management of carotid and vertebral spontaneous and traumatic dissection. Angiology. doi:10.1177/0003319712475154

    PubMed  Google Scholar 

  39. Stevic I, Chan HH, Chan AK (2011) Carotid artery dissections: thrombosis of the false lumen. Thromb Res 128:317–324

    Article  PubMed  CAS  Google Scholar 

  40. Marder VJ, Chute DJ, Starkman S, Abolian AM, Kidwell C, Liebeskind D, Ovbiagele B, Vinuela F, Duckwiler G, Jahan R, Vespa PM, Selco S, Rajajee V, Kim D, Sanossian N, Saver JL (2006) Analysis of thrombi retrieved from cerebral arteries of patients with acute ischemic stroke. Stroke 37:2086–2093

    Article  PubMed  Google Scholar 

  41. Almekhlafi MA, Hu WY, Hill MD, Auer RN (2008) Calcification and endothelialization of thrombi in acute stroke. Ann Neurol 64:344–348

    Article  PubMed  Google Scholar 

  42. Bhatia R, Hill MD, Shobha N, Menon B, Bal S, Kochar P, Watson T, Goyal M, Demchuk AM (2010) Low rates of acute recanalization with intravenous recombinant tissue plasminogen activator in ischemic stroke: real-world experience and a call for action. Stroke 41:2254–2258

    Article  PubMed  CAS  Google Scholar 

  43. Khatri P, Abruzzo T, Yeatts SD, Nichols C, Broderick JP, Tomsick TA (2009) Good clinical outcome after ischemic stroke with successful revascularization is time-dependent. Neurology 73:1066–1072

    Article  PubMed  CAS  Google Scholar 

  44. Wu JH, Siddiqui K, Diamond SL (1994) Transport phenomena and clot dissolving therapy: an experimental investigation of diffusion-controlled and permeation-enhanced fibrinolysis. Thromb Haemost 72:105–112

    PubMed  CAS  Google Scholar 

  45. Blinc A, Keber D, Lahajnar G, Stegnar M, Zidansek A, Demsar F (1992) Lysing patterns of retracted blood clots with diffusion or bulk flow transport of plasma with urokinase into clots—a magnetic resonance imaging study in vitro. Thromb Haemost 68:667–671

    PubMed  CAS  Google Scholar 

  46. Moftakhar P, English JD, Cooke DL, Kim WT, Stout C, Smith WS, Dowd CF, Higashida RT, Halbach VV, Hetts SW (2013) Density of thrombus on admission ct predicts revascularization efficacy in large vessel occlusion acute ischemic stroke. Stroke 44:243–245

    Article  PubMed  Google Scholar 

  47. Rocha S, Pires A, Gomes J, Rocha J, Sousa F, Pinho J, Rodrigues M, Ferreira C, Machado A, Mare R, Fontes JR (2011) Intravenous thrombolysis is more effective in ischemic cardioembolic strokes than in non-cardioembolic? Arq Neuropsiquiatr 69:905–909

    Article  PubMed  Google Scholar 

  48. Hsia AW, Sachdev HS, Tomlinson J, Hamilton SA, Tong DC (2003) Efficacy of IV tissue plasminogen activator in acute stroke: does stroke subtype really matter? Neurology 61:71–75

    Article  PubMed  CAS  Google Scholar 

  49. Mustanoja S, Meretoja A, Putaala J, Viitanen V, Curtze S, Atula S, Artto V, Happola O, Kaste M (2011) Outcome by stroke etiology in patients receiving thrombolytic treatment: descriptive subtype analysis. Stroke 42:102–106

    Article  PubMed  CAS  Google Scholar 

  50. Grau AJ, Weimar C, Buggle F, Heinrich A, Goertler M, Neumaier S, Glahn J, Brandt T, Hacke W, Diener HC (2001) Risk factors, outcome, and treatment in subtypes of ischemic stroke: the German stroke data bank. Stroke 32:2559–2566

    Article  PubMed  CAS  Google Scholar 

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We declare that we have no conflict of interest.

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Correspondence to J. M. Niesten.

Additional information

The following individuals and institutions constitute the DUST Study University Medical Center Utrecht, The Netherlands Department of Radiology B.K. Velthuis, T. van Seeters, I.C. van der Schaaf, J.M. Niesten, J.W. Dankbaar, W.P.T.M. Mali; Department of Neurology M.J.A. Luitse, G.J. Biessels, L.J. Kappelle; Julius Center for Health Sciences and Primary Care Y. van der Graaf; Academic Medical Center Amsterdam, The Netherlands Department of Radiology C.B.L.M. Majoie, L.F.M. Beenen; Department of Neurology Y.B. Roos; Catharina Hospital Eindhoven, The Netherlands Department of Radiology L.E.M. Duijm; Department of Neurology K. Keizer; Erasmus Medical Center Rotterdam, The Netherlands Department of Radiology A. van der Lugt; Department of Neurology D.W.J. Dippel; Gelre Hospital Apeldoorn, The Netherlands Department of Radiology K.E. Droogh-de Greeve; Department of Neurology H.P. Bienfait; Leiden University Medical Center, The Netherlands Department of Radiology M.A.A. van Walderveen Department of Neurology M.J.H. Wermer; Medical Center Leeuwarden, The Netherlands Department of Radiology J. Dol; Department of Neurology W.J. Schuiling; Medical Center Haaglanden Den Haag, The Netherlands Department of Radiology G.J. Lycklama à Nijeholt; Department of Neurology J. Boiten; Onze Lieve Vrouwe Gasthuis Amsterdam, The Netherlands Department of Radiology D. Duyndam; Department of Neurology V.I.H. Kwa; Radboud University Nijmegen Medical Center, The Netherlands Department of Radiology A. Meijer; Department of Neurology E.J. van Dijk; Rijnstate Hospital Arnhem, The Netherlands Department of Radiology F.O.H.W. Kesselring, A.D. Horsch; Department of Neurology J. Hofmeijer; St. Antonius Hospital Nieuwegein, The Netherlands Department of Radiology J.A. Vos; Department of Neurology W.J. Schonewille; St. Elisabeth Hospital Tilburg, The Netherlands Department of Radiology W.J. van Rooij; Department of Neurology P.L.M. de Kort; St. Franciscus Hospital Rotterdam, The Netherlands; Department of Radiology C.C. Pleiter; Department of Neurology S.L.M. Bakker; VU Medical Center Amsterdam, The Netherlands Department of Radiology J. Bot; Department of Neurology M.C. Visser

Clinical Trial Registration Information URL: http://www.ClinicalTrials.gov.Unique-identifierNCT00880113

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Niesten, J.M., van der Schaaf, I.C., Biessels, G.J. et al. Relationship between thrombus attenuation and different stroke subtypes. Neuroradiology 55, 1071–1079 (2013). https://doi.org/10.1007/s00234-013-1217-y

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