Immunohistochemical analysis of cerebral thrombi retrieved by mechanical thrombectomy from patients with acute ischemic stroke

International Journal of Molecular Sciences

Volumn 17, Issue 3, 2016, Pages

  Schuhmann, Michael K ^a   Gunreben, Ignaz ^a   Kleinschnitz, Christoph ^a   Kraft, Peter ^a  

^a UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

Immune cells; Inflammation; Ischemic stroke; Lymphocytes; Mechanical thrombectomy; Thrombus formation

Indexed keywords

COLLAGEN; FIBRIN; VON WILLEBRAND FACTOR; BIOLOGICAL MARKER;

ADULT; AGED; ARTICLE; BLOOD ANALYSIS; BRAIN ISCHEMIA; CD4+ T LYMPHOCYTE; CD68+ MONOCYTE; CLINICAL ARTICLE; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; MALE; MECHANICAL THROMBECTOMY; MIDDLE AGED; MONOCYTE; NATIONAL INSTITUTES OF HEALTH STROKE SCALE; T LYMPHOCYTE; THROMBOCYTE; THROMBUS; VERY ELDERLY; LYMPHOCYTE; METABOLISM; PATHOLOGY; STROKE; THROMBECTOMY; THROMBOSIS;

ADULT; AGED; AGED, 80 AND OVER; BIOMARKERS; BRAIN ISCHEMIA; FEMALE; FIBRIN; HUMANS; LYMPHOCYTES; MALE; MIDDLE AGED; STROKE; THROMBECTOMY; THROMBOSIS; VON WILLEBRAND FACTOR;

EID: 84959210391     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17030298     Document Type: Article

References (47)

1. Berkhemer, O.A.; Fransen, P.S.; Beumer, D.; van den Berg, L.A.; Lingsma, H.F.; Yoo, A.J.; Schonewille, W.J.; Vos, J.A.; Nederkoorn, P.J.; Wermer, M.J. et al. A randomized trial of intraarterial treatment for acute ischemic stroke. N. Engl. J. Med. 2015, 372, 11–20. [CrossRef][PubMed]
2. Campbell, B.C.; Mitchell, P.J.; Investigators, E.I. Endovascular therapy for ischemic stroke. N. Engl. J. Med. 2015, 372, 2365–2366. [CrossRef][PubMed]
3. Jovin, T.G.; Chamorro, A.; Cobo, E.; de Miquel, M.A.; Molina, C.A.; Rovira, A.; San Roman, L.; Serena, J.; Abilleira, S.; Ribo, M. et al. Thrombectomy within 8 hours after symptom onset in ischemic stroke. N. Engl. J. Med. 2015, 372, 2296–2306. [CrossRef][PubMed]
4. Jauch, E.C.; Saver, J.L.; Adams, H.P., Jr.; Bruno, A.; Connors, J.J.; Demaerschalk, B.M.; Khatri, P.; McMullan, P.W., Jr.; Qureshi, A.I.; Rosenfield, K. et al. Guidelines for the early management of patients with acute ischemic stroke: A guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2013, 44, 870–947. [CrossRef][PubMed]
5. Riedel, C.H.; Zimmermann, P.; Jensen-Kondering, U.; Stingele, R.; Deuschl, G.; Jansen, O. The importance of size: Successful recanalization by intravenous thrombolysis in acute anterior stroke depends on thrombus length. Stroke 2011, 42, 1775–1777. [CrossRef][PubMed]
6. Jindal, G.; Miller, T.; Shivashankar, R.; Mitchell, J.; Stern, B.J.; Yarbrough, K.; Gandhi, D. Relationship of thrombus length to number of stent retrievals, revascularization, and outcomes in acute ischemic stroke. J. Vasc. Interv. Radiol. 2014, 25, 1549–1557. [CrossRef][PubMed]
7. Puig, J.; Pedraza, S.; Demchuk, A.; Daunis, I.E.J.; Termes, H.; Blasco, G.; Soria, G.; Boada, I.; Remollo, S.; Banos, J. et al. Quantification of thrombus hounsfield units on noncontrast CT predicts stroke subtype and early recanalization after intravenous recombinant tissue plasminogen activator. Am. J. Neuroradiol. 2012, 33, 90–96. [CrossRef][PubMed]
8. Moftakhar, P.; English, J.D.; Cooke, D.L.; Kim, W.T.; Stout, C.; Smith, W.S.; Dowd, C.F.; Higashida, R.T.; Halbach, V.V.; Hetts, S.W. Density of thrombus on admission CT predicts revascularization efficacy in large vessel occlusion acute ischemic stroke. Stroke 2013, 44, 243–245. [CrossRef][PubMed]
9. Mokin, M.; Morr, S.; Natarajan, S.K.; Lin, N.; Snyder, K.V.; Hopkins, L.N.; Siddiqui, A.H.; Levy, E.I. Thrombus density predicts successful recanalization with Solitaire stent retriever thrombectomy in acute ischemic stroke. J. Neurointerv. Surg. 2015, 7, 104–107. [CrossRef][PubMed]
10. Jorgensen, L.; Torvik, A. Ischaemic cerebrovascular diseases in an autopsy series: Part 1. Prevalence, location and predisposing factors in verified thrombo-embolic occlusions, and their significance in the pathogenesis of cerebral infarction. J. Neurol. Sci. 1966, 3, 490–509. [CrossRef]
11. Marder, V.J.; Chute, D.J.; Starkman, S.; Abolian, A.M.; Kidwell, C.; Liebeskind, D.; Ovbiagele, B.; Vinuela, F.; Duckwiler, G.; Jahan, R. et al. Analysis of thrombi retrieved from cerebral arteries of patients with acute ischemic stroke. Stroke 2006, 37, 2086–2093. [CrossRef][PubMed]
12. Niesten, J.M.; van der Schaaf, I.C.; van Dam, L.; Vink, A.; Vos, J.A.; Schonewille, W.J.; de Bruin, P.C.; Mali, W.P.; Velthuis, B.K. Histopathologic composition of cerebral thrombi of acute stroke patients is correlated with stroke subtype and thrombus attenuation. PLoS ONE 2014, 9, e88882. [CrossRef][PubMed]
13. Liebeskind, D.S.; Sanossian, N.; Yong, W.H.; Starkman, S.; Tsang, M.P.; Moya, A.L.; Zheng, D.D.; Abolian, A.M.; Kim, D.; Ali, L.K. et al. CT and MRI early vessel signs reflect clot composition in acute stroke. Stroke 2011, 42, 1237–1243. [CrossRef][PubMed]
14. Kim, S.K.; Yoon, W.; Kim, T.S.; Kim, H.S.; Heo, T.W.; Park, M.S. Histologic Analysis of Retrieved Clots in Acute Ischemic Stroke: Correlation with Stroke Etiology and Gradient-Echo MRI. Am. J. Neuroradiol. 2015, 36, 1756–1762. [CrossRef][PubMed]
15. Boeckh-Behrens, T.; Schubert, M.; Forschler, A.; Prothmann, S.; Kreiser, K.; Zimmer, C.; Riegger, J.; Bauer, J.; Neff, F.; Kehl, V. et al. The Impact of Histological Clot Composition in Embolic Stroke. Clin. Neuroradiol. 2014, 1–9. [CrossRef][PubMed]
16. Liebeskind, D.S.; Jahan, R.; Nogueira, R.G.; Jovin, T.G.; Lutsep, H.L.; Saver, J.L.; Investigators, S. Serial Alberta Stroke Program early CT score from baseline to 24 hours in Solitaire Flow Restoration with the Intention for Thrombectomy study: A novel surrogate end point for revascularization in acute stroke. Stroke 2014, 45, 723–727. [CrossRef][PubMed]
17. Niesten, J.M.; van der Schaaf, I.C.; Biessels, G.J.; van Otterloo, A.E.; van Seeters, T.; Horsch, A.D.; Luitse, M.J.; van der Graaf, Y.; Kappelle, L.J.; Mali, W.P. et al. Relationship between thrombus attenuation and different stroke subtypes. Neuroradiology 2013, 55, 1071–1079. [CrossRef][PubMed]
18. Simons, N.; Mitchell, P.; Dowling, R.; Gonzales, M.; Yan, B. Thrombus composition in acute ischemic stroke: A histopathological study of thrombus extracted by endovascular retrieval. J. Neuroradiol. 2015, 42, 86–92. [CrossRef][PubMed]
19. Minnerup, J.; Kleinschnitz, C. Visualization of clot composition in ischemic stroke: Do we get what we see? Stroke 2011, 42, 1193–1194. [CrossRef][PubMed]
20. Von zur Muhlen, C.; von Elverfeldt, D.; Moeller, J.A.; Choudhury, R.P.; Paul, D.; Hagemeyer, C.E.; Olschewski, M.; Becker, A.; Neudorfer, I.; Bassler, N. et al. Magnetic resonance imaging contrast agent targeted toward activated platelets allows in vivo detection of thrombosis and monitoring of thrombolysis. Circulation 2008, 118, 258–267. [CrossRef][PubMed]
21. Overoye-Chan, K.; Koerner, S.; Looby, R.J.; Kolodziej, A.F.; Zech, S.G.; Deng, Q.; Chasse, J.M.; McMurry, T.J.; Caravan, P. EP-2104R: A fibrin-specific gadolinium-Based MRI contrast agent for detection of thrombus. J. Am. Chem. Soc. 2008, 130, 6025–6039. [CrossRef][PubMed]
22. Spuentrup, E.; Botnar, R.M.; Wiethoff, A.J.; Ibrahim, T.; Kelle, S.; Katoh, M.; Ozgun, M.; Nagel, E.; Vymazal, J.; Graham, P.B. et al. MR imaging of thrombi using EP-2104R, a fibrin-specific contrast agent: Initial results in patients. Eur. Radiol. 2008, 18, 1995–2005. [CrossRef][PubMed]
23. Yilmaz, G.; Arumugam, T.V.; Stokes, K.Y.; Granger, D.N. Role of T lymphocytes and interferon-gamma in ischemic stroke. Circulation 2006, 113, 2105–2112. [CrossRef][PubMed]
24. Kleinschnitz, C.; Kraft, P.; Dreykluft, A.; Hagedorn, I.; Gobel, K.; Schuhmann, M.K.; Langhauser, F.; Helluy, X.; Schwarz, T.; Bittner, S. et al. Regulatory T cells are strong promoters of acute ischemic stroke in mice by inducing dysfunction of the cerebral microvasculature. Blood 2013, 121, 679–691. [CrossRef][PubMed]
25. Kleinschnitz, C.; Schwab, N.; Kraft, P.; Hagedorn, I.; Dreykluft, A.; Schwarz, T.; Austinat, M.; Nieswandt, B.; Wiendl, H.; Stoll, G. Early detrimental T-cell effects in experimental cerebral ischemia are neither related to adaptive immunity nor thrombus formation. Blood 2010, 115, 3835–3842. [CrossRef][PubMed]
26. Kraft, P.; Gob, E.; Schuhmann, M.K.; Gobel, K.; Deppermann, C.; Thielmann, I.; Herrmann, A.M.; Lorenz, K.; Brede, M.; Stoll, G. et al. FTY720 ameliorates acute ischemic stroke in mice by reducing thrombo-inflammation but not by direct neuroprotection. Stroke 2013, 44, 3202–3210. [CrossRef][PubMed]
27. Nieswandt, B.; Kleinschnitz, C.; Stoll, G. Ischaemic stroke: A thrombo-inflammatory disease? J. Physiol. 2011, 589, 4115–4123. [CrossRef][PubMed]
28. Smout, J.; Dyker, A.; Cleanthis, M.; Ford, G.; Kesteven, P.; Stansby, G. Platelet function following acute cerebral ischemia. Angiology 2009, 60, 362–369. [CrossRef][PubMed]
29. Htun, P.; Fateh-Moghadam, S.; Tomandl, B.; Handschu, R.; Klinger, K.; Stellos, K.; Garlichs, C.; Daniel, W. Gawaz, M. Course of platelet activation and platelet-leukocyte interaction in cerebrovascular ischemia. Stroke 2006, 37, 2283–2287. [CrossRef][PubMed]
30. Zhu, Z.; Fu, Y.; Tian, D.; Sun, N.; Han, W.; Chang, G.; Dong, Y.; Xu, X.; Liu, Q.; Huang, D.; et al. Combination of the Immune Modulator FingolimodWith Alteplase in Acute Ischemic Stroke: A Pilot Trial. Circulation 2015, 132, 1104–1112. [CrossRef][PubMed]
31. Muir, K.W.; Weir, C.J.; Murray, G.D.; Povey, C.; Lees, K.R. Comparison of neurological scales and scoring systems for acute stroke prognosis. Stroke 1996, 27, 1817–1820. [CrossRef][PubMed]
32. 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. [CrossRef][PubMed]
33. Higashida, R.T.; Furlan, A.J.; Roberts, H.; Tomsick, T.; Connors, B.; Barr, J.; Dillon, W.; Warach, S.; Broderick, J.; Tilley, B. et al. Trial design and reporting standards for intra-arterial cerebral thrombolysis for acute ischemic stroke. Stroke 2003, 34, e109–e137. [CrossRef][PubMed]
34. Benakis, C.; Garcia-Bonilla, L.; Iadecola, C.; Anrather, J. The role of microglia and myeloid immune cells in acute cerebral ischemia. Front. Cell. Neurosci. 2014, 8, 461. [CrossRef][PubMed]
35. Ahrens, E.T.; Bulte, J.W. Tracking immune cells in vivo using magnetic resonance imaging. Nat. Rev. Immunol. 2013, 13, 755–763. [CrossRef][PubMed]
36. Jacobin-Valat, M.J.; Laroche-Traineau, J.; Lariviere, M.; Mornet, S.; Sanchez, S.; Biran, M.; Lebaron, C.; Boudon, J.; Lacomme, S.; Cerutti, M. et al. Nanoparticles functionalised with an anti-platelet human antibody for in vivo detection of atherosclerotic plaque by magnetic resonance imaging. Nanomedicine 2015, 11, 927–937. [CrossRef][PubMed]
37. Kraft, P.; Drechsler, C.; Schuhmann, M.K.; Gunreben, I.; Kleinschnitz, C. Characterization of Peripheral Immune Cell Subsets in Patients with Acute and Chronic Cerebrovascular Disease: A Case-Control Study. Int. J. Mol. Sci. 2015, 16, 25433–25449. [CrossRef][PubMed]
38. Fu, Y.; Liu, Q.; Anrather, J.; Shi, F.D. Immune interventions in stroke. Nat. Rev. Immunol. 2015, 11, 524–535. [CrossRef][PubMed]
39. Rinder, H.M.; Bonan, J.L.; Rinder, C.S.; Ault, K.A.; Smith, B.R. Dynamics of leukocyte-platelet adhesion in whole blood. Blood 1991, 78, 1730–1737. [PubMed]
40. Jin, R.; Yang, G.; Li, G. Inflammatory mechanisms in ischemic stroke: Role of inflammatory cells. J. Leukoc. Biol. 2010, 87, 779–789. [CrossRef][PubMed]
41. Pende, A.; Artom, N.; Bertolotto, M.; Montecucco, F.; Dallegri, F. Role of Neutrophils in Atherogenesis: An Update. Eur. J. Clin. Investig. 2016, 46, 252–263. [CrossRef][PubMed]
42. Idzkowska, E.; Eljaszewicz, A.; Miklasz, P.; Musial, W.J.; Tycinska, A.M.; Moniuszko, M. The Role of Different Monocyte Subsets in the Pathogenesis of Atherosclerosis and Acute Coronary Syndromes. Scand. J. Immunol. 2015, 82, 163–173. [CrossRef][PubMed]
43. Zernecke, A. Dendritic cells in atherosclerosis: Evidence in mice and humans. Arterioscler. Thromb. Vasc. Biol. 2015, 35, 763–770. [CrossRef][PubMed]
44. Makris, G.C.; Teng, Z.; Patterson, A.J.; Lin, J.M.; Young, V.; Graves, M.J.; Gillard, J.H. Advances in MRI for the evaluation of carotid atherosclerosis. Br. J Radiol. 2015, 88, 20140282. [CrossRef][PubMed]
45. Alie, N.; Eldib, M.; Fayad, Z.A.; Mani, V. Inflammation, Atherosclerosis, and Coronary Artery Disease: PET/CT for the Evaluation of Atherosclerosis and Inflammation. Clin. Med. Insights Cardiol. 2014, 8 (3), S13–S21.
46. Singh, P.; Doostkam, S.; Reinhard, M.; Ivanovas, V.; Taschner, C.A. Immunohistochemical analysis of thrombi retrieved during treatment of acute ischemic stroke: Does stent-retriever cause intimal damage? Stroke 2013, 44, 1720–1722. [CrossRef][PubMed]
47. Mohlenbruch, M.; Stampfl, S.; Behrens, L.; Herweh, C.; Rohde, S.; Bendszus, M.; Hametner, C.; Nagel, S.; Ringleb, P.A.; Pham, M. Mechanical thrombectomy with stent retrievers in acute basilar artery occlusion. Am. J. Neuroradiol. 2014, 35, 959–964. [CrossRef][PubMed]