Tailoring specific interventions according to the type of thrombus: can neuroimaging help?

By Barbara Casolla, MD, PhD, Univ. Lille, Inserm U1171, Degenerative and Vascular Cognitive Disorders, CHU Lille, Department of Neurology, France
Twitter: @BarbaraCasolla

In 1983, Gács et al. reported the “hyperdense cerebral artery sign” as the earliest neuroimaging sign of acute ischemic stroke1, visible long before early ischemic parenchymal changes. This sign is present in about 40% of patients with a middle cerebral artery infarct, and it has a specificity of 100% and a sensibility of 30%2. Indeed, thrombus corresponds to higher local hematocrit level, due to extrusion of plasma from clotted cells within, explaining the increasing of Hounsfield unit (HU) on non-contrast computed tomography (CT).

Up-to-date, CT/CT-angiography(CTA) thrombus characterization has improved and brings hints for therapeutic choices and prognosis prediction. Indeed, beyond thrombus location, multiple other parameter related to thrombus characteristics, such as thrombus perviousness3, length4 and volume5, can be evaluated in the acute setting. The Clot Burden Score6, a CTA-based grading system has been successively developed, and reflects thrombus extent and location in the cerebral anterior circulation. Longer thrombus and more proximal location gained lower scores in this 10-point scoring system, and strongly predicted low successful recanalization rates and poor clinical outcome7–9.

Available data suggest that CT parameters can help decision strategies for reperfusion therapies: before starting mechanical thrombectomy, clot dimensions could allow planning the endovascular procedure with the appropriate size and length of stent retriever, increasing the rate of first-pass recanalization and obtaining higher likelihood of a favourable outcome8.

Moreover, clot histology predicts tissue plasminogen activator(rtPA)-mediated intravenous thrombolysis (IVT) resistance, with red blood cell-rich area being more drug permeable and rtPA susceptible. Susceptibility vessel sign (SVS) on T2* magnetic resonance imaging (MRI) and SusceptibilityWeighed Imaging (SWI) sequences is related to the presence of deoxyhemoglobin, which determines a strong paramagnetic effect determining a signal loss on T2*sequences (Figure).

Indeed, SVS presence seems to correlate with an RBC-dominant thrombus, with variable diagnostic accuracy10. Recently, thrombus T2* relaxation time (R2*) has been proposed as a method of quantitative evaluation of thrombus composition11 and texture analysis of MRI-R2* maps can potentially estimate the clot content of red blood cell and iron12. Indeed, it is likely that neuroimaging studies on correlations with histological composition may contribute, in the future, to select patients for clinical trials on new targeted lytic therapies13.

Figure: Left middle cerebral artery proximal occlusion on Time of flight (TOF) MRI sequence (left) and T2* sequence (right), showing the susceptibility vessel sign (white arrow).

Consistently with CT data, Clot Burden Score on admission T2*-MRI has been shown to significantly predict recanalization and 3-month outcome after intravenous thrombolysis14 and thrombus length predicted early recanalization after IVT in patients with minor stroke and large vessel occlusion15.

Thrombus characterisation by non-invasive neuroimaging provides transversal and clinically relevant data. Research should be boosted more than it has been since the description of hyperdense cerebral artery sign, 37 years ago. Indeed, imaging/histology correlations may have a role in driving personalized reperfusion strategies in the acute phase, significantly increasing their efficacy, and could also bring clues in routine practice to predict stroke etiology.

 

Acknowledgments: 

Dr Gregory Kuchcinski, Department of Neuroradiology, Lille University Hospital, France

Dr François Caparros, Department of Neurology, Stroke Unit, Lille University Hospital, France

 

References

  1. Gács G, Fox AJ, Barnett HJ, Vinuela F. CT visualization of intracranial arterial thromboembolism. Stroke. 1983;14:756–762.
  2. Leys D, Pruvo JP, Godefroy O, Rondepierre P, Leclerc X. Prevalence and significance of hyperdense middle cerebral artery in acute stroke. Stroke. 1992;23:317–324.
  3. Santos EMM, Marquering HA, den Blanken MD, Berkhemer OA, Boers AMM, Yoo AJ, et al. Thrombus Permeability Is Associated With Improved Functional Outcome and Recanalization in Patients With Ischemic Stroke. Stroke. 2016;47:732–741.
  4. Polito V, La Piana R, Del Pilar Cortes M, Tampieri D. Assessment of clot length with multiphase CT angiography in patients with acute ischemic stroke. Neuroradiol J. 2017;30:593–599.
  5. Yoo J, Baek J-H, Park H, Song D, Kim K, Hwang IG, et al. Thrombus Volume as a Predictor of Nonrecanalization After Intravenous Thrombolysis in Acute Stroke. Stroke. 2018;49:2108–2115.
  6. Puetz V, Dzialowski I, Hill MD, Subramaniam S, Sylaja PN, Krol A, et al. Intracranial thrombus extent predicts clinical outcome, final infarct size and hemorrhagic transformation in ischemic stroke: the clot burden score. Int J Stroke. 2008;3:230–236.
  7. Li G, Wu G, Qin Z, Li H, Cheng X, Cai Y. Prognostic Value of Clot Burden Score in Acute Ischemic Stroke after Reperfusion Therapies: A Systematic Review and Meta-Analysis. J Stroke Cerebrovasc Dis. 2019;28:104293.
  8. Baek J-H, Yoo J, Song D, Kim YD, Nam HS, Kim BM, et al. Predictive value of thrombus volume for recanalization in stent retriever thrombectomy. Sci Rep. 2017;7:15938.
  9. Riedel CH, 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.
  10. Bourcier R, Détraz L, Serfaty JM, Delasalle BG, Mirza M, Derraz I, et al. MRI Interscanner Agreement of the Association between the Susceptibility Vessel Sign and Histologic Composition of Thrombi. J Neuroimaging. 2017;27:577–582.
  11. Bourcier R, Pautre R, Mirza M, Castets C, Darcourt J, Labreuche J, et al. MRI Quantitative T2* Mapping to Predict Dominant Composition of In Vitro Thrombus. AJNR Am J Neuroradiol. 2019;40:59–64.
  12. Bretzner M, Lopes R, McCarthy R, Corseaux D, Auger F, Gunning G, et al. Texture parameters of R2* maps are correlated with iron concentration and red blood cells count in clot analogs: A 7-T micro-MRI study. J Neuroradiol. 2019;
  13. Janot K, Zhu F, Kerleroux B, Boulouis G, Shotar E, Premat K, et al. “Adaptative endovascular strategy to the CloT MRI in large intracranial vessel occlusion” (VECTOR): Study protocol of a randomized control trial. J Neuroradiol. 2019;
  14. Legrand L, Naggara O, Turc G, Mellerio C, Roca P, Calvet D, et al. Clot Burden Score on Admission T2*-MRI Predicts Recanalization in Acute Stroke. Stroke. 2013;44:1878–1884.
  15. Seners P, Delepierre J, Turc G, Henon H, Piotin M, Arquizan C, et al. Thrombus Length Predicts Lack of Post-Thrombolysis Early Recanalization in Minor Stroke With Large Vessel Occlusion. Stroke. 2019;50:761–764.

 

Tailoring specific interventions according to the type of thrombus: can neuroimaging help?

By Barbara Casolla, MD, PhD, Univ. Lille, Inserm U1171, Degenerative and Vascular Cognitive Disorders, CHU Lille, Department of Neurology, France
Twitter: @BarbaraCasolla

In 1983, Gács et al. reported the “hyperdense cerebral artery sign” as the earliest neuroimaging sign of acute ischemic stroke1, visible long before early ischemic parenchymal changes. This sign is present in about 40% of patients with a middle cerebral artery infarct, and it has a specificity of 100% and a sensibility of 30%2. Indeed, thrombus corresponds to higher local hematocrit level, due to extrusion of plasma from clotted cells within, explaining the increasing of Hounsfield unit (HU) on non-contrast computed tomography (CT).

Up-to-date, CT/CT-angiography(CTA) thrombus characterization has improved and brings hints for therapeutic choices and prognosis prediction. Indeed, beyond thrombus location, multiple other parameter related to thrombus characteristics, such as thrombus perviousness3, length4 and volume5, can be evaluated in the acute setting. The Clot Burden Score6, a CTA-based grading system has been successively developed, and reflects thrombus extent and location in the cerebral anterior circulation. Longer thrombus and more proximal location gained lower scores in this 10-point scoring system, and strongly predicted low successful recanalization rates and poor clinical outcome7–9.

Available data suggest that CT parameters can help decision strategies for reperfusion therapies: before starting mechanical thrombectomy, clot dimensions could allow planning the endovascular procedure with the appropriate size and length of stent retriever, increasing the rate of first-pass recanalization and obtaining higher likelihood of a favourable outcome8.

Moreover, clot histology predicts tissue plasminogen activator(rtPA)-mediated intravenous thrombolysis (IVT) resistance, with red blood cell-rich area being more drug permeable and rtPA susceptible. Susceptibility vessel sign (SVS) on T2* magnetic resonance imaging (MRI) and SusceptibilityWeighed Imaging (SWI) sequences is related to the presence of deoxyhemoglobin, which determines a strong paramagnetic effect determining a signal loss on T2*sequences (Figure).

Indeed, SVS presence seems to correlate with an RBC-dominant thrombus, with variable diagnostic accuracy10. Recently, thrombus T2* relaxation time (R2*) has been proposed as a method of quantitative evaluation of thrombus composition11 and texture analysis of MRI-R2* maps can potentially estimate the clot content of red blood cell and iron12. Indeed, it is likely that neuroimaging studies on correlations with histological composition may contribute, in the future, to select patients for clinical trials on new targeted lytic therapies13.

 

Consistently with CT data, Clot Burden Score on admission T2*-MRI has been shown to significantly predict recanalization and 3-month outcome after intravenous thrombolysis14 and thrombus length predicted early recanalization after IVT in patients with minor stroke and large vessel occlusion15.

Thrombus characterisation by non-invasive neuroimaging provides transversal and clinically relevant data. Research should be boosted more than it has been since the description of hyperdense cerebral artery sign, 37 years ago. Indeed, imaging/histology correlations may have a role in driving personalized reperfusion strategies in the acute phase, significantly increasing their efficacy, and could also bring clues in routine practice to predict stroke etiology.

 

 

Acknowledgments: 

Dr Gregory Kuchcinski, Department of Neuroradiology, Lille University Hospital, France

Dr François Caparros, Department of Neurology, Stroke Unit, Lille University Hospital, France

 

 

References

 

  1. Gács G, Fox AJ, Barnett HJ, Vinuela F. CT visualization of intracranial arterial thromboembolism. Stroke. 1983;14:756–762.
  2. Leys D, Pruvo JP, Godefroy O, Rondepierre P, Leclerc X. Prevalence and significance of hyperdense middle cerebral artery in acute stroke. Stroke. 1992;23:317–324.
  3. Santos EMM, Marquering HA, den Blanken MD, Berkhemer OA, Boers AMM, Yoo AJ, et al. Thrombus Permeability Is Associated With Improved Functional Outcome and Recanalization in Patients With Ischemic Stroke. Stroke. 2016;47:732–741.
  4. Polito V, La Piana R, Del Pilar Cortes M, Tampieri D. Assessment of clot length with multiphase CT angiography in patients with acute ischemic stroke. Neuroradiol J. 2017;30:593–599.
  5. Yoo J, Baek J-H, Park H, Song D, Kim K, Hwang IG, et al. Thrombus Volume as a Predictor of Nonrecanalization After Intravenous Thrombolysis in Acute Stroke. Stroke. 2018;49:2108–2115.
  6. Puetz V, Dzialowski I, Hill MD, Subramaniam S, Sylaja PN, Krol A, et al. Intracranial thrombus extent predicts clinical outcome, final infarct size and hemorrhagic transformation in ischemic stroke: the clot burden score. Int J Stroke. 2008;3:230–236.
  7. Li G, Wu G, Qin Z, Li H, Cheng X, Cai Y. Prognostic Value of Clot Burden Score in Acute Ischemic Stroke after Reperfusion Therapies: A Systematic Review and Meta-Analysis. J Stroke Cerebrovasc Dis. 2019;28:104293.
  8. Baek J-H, Yoo J, Song D, Kim YD, Nam HS, Kim BM, et al. Predictive value of thrombus volume for recanalization in stent retriever thrombectomy. Sci Rep. 2017;7:15938.
  9. Riedel CH, 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.
  10. Bourcier R, Détraz L, Serfaty JM, Delasalle BG, Mirza M, Derraz I, et al. MRI Interscanner Agreement of the Association between the Susceptibility Vessel Sign and Histologic Composition of Thrombi. J Neuroimaging. 2017;27:577–582.
  11. Bourcier R, Pautre R, Mirza M, Castets C, Darcourt J, Labreuche J, et al. MRI Quantitative T2* Mapping to Predict Dominant Composition of In Vitro Thrombus. AJNR Am J Neuroradiol. 2019;40:59–64.
  12. Bretzner M, Lopes R, McCarthy R, Corseaux D, Auger F, Gunning G, et al. Texture parameters of R2* maps are correlated with iron concentration and red blood cells count in clot analogs: A 7-T micro-MRI study. J Neuroradiol. 2019;
  13. Janot K, Zhu F, Kerleroux B, Boulouis G, Shotar E, Premat K, et al. “Adaptative endovascular strategy to the CloT MRI in large intracranial vessel occlusion” (VECTOR): Study protocol of a randomized control trial. J Neuroradiol. 2019;
  14. Legrand L, Naggara O, Turc G, Mellerio C, Roca P, Calvet D, et al. Clot Burden Score on Admission T2*-MRI Predicts Recanalization in Acute Stroke. Stroke. 2013;44:1878–1884.
  15. Seners P, Delepierre J, Turc G, Henon H, Piotin M, Arquizan C, et al. Thrombus Length Predicts Lack of Post-Thrombolysis Early Recanalization in Minor Stroke With Large Vessel Occlusion. Stroke. 2019;50:761–764.

Tailoring specific interventions according to the type of thrombus: can neuroimaging help?

By Barbara Casolla, MD, PhD, Univ. Lille, Inserm U1171, Degenerative and Vascular Cognitive Disorders, CHU Lille, Department of Neurology, France
Twitter: @BarbaraCasolla

In 1983, Gács et al. reported the “hyperdense cerebral artery sign” as the earliest neuroimaging sign of acute ischemic stroke1, visible long before early ischemic parenchymal changes. This sign is present in about 40% of patients with a middle cerebral artery infarct, and it has a specificity of 100% and a sensibility of 30%2. Indeed, thrombus corresponds to higher local hematocrit level, due to extrusion of plasma from clotted cells within, explaining the increasing of Hounsfield unit (HU) on non-contrast computed tomography (CT).

Up-to-date, CT/CT-angiography(CTA) thrombus characterization has improved and brings hints for therapeutic choices and prognosis prediction. Indeed, beyond thrombus location, multiple other parameter related to thrombus characteristics, such as thrombus perviousness3, length4 and volume5, can be evaluated in the acute setting. The Clot Burden Score6, a CTA-based grading system has been successively developed, and reflects thrombus extent and location in the cerebral anterior circulation. Longer thrombus and more proximal location gained lower scores in this 10-point scoring system, and strongly predicted low successful recanalization rates and poor clinical outcome7–9.

Available data suggest that CT parameters can help decision strategies for reperfusion therapies: before starting mechanical thrombectomy, clot dimensions could allow planning the endovascular procedure with the appropriate size and length of stent retriever, increasing the rate of first-pass recanalization and obtaining higher likelihood of a favourable outcome8.

Moreover, clot histology predicts tissue plasminogen activator(rtPA)-mediated intravenous thrombolysis (IVT) resistance, with red blood cell-rich area being more drug permeable and rtPA susceptible. Susceptibility vessel sign (SVS) on T2* magnetic resonance imaging (MRI) and SusceptibilityWeighed Imaging (SWI) sequences is related to the presence of deoxyhemoglobin, which determines a strong paramagnetic effect determining a signal loss on T2*sequences (Figure).

Indeed, SVS presence seems to correlate with an RBC-dominant thrombus, with variable diagnostic accuracy10. Recently, thrombus T2* relaxation time (R2*) has been proposed as a method of quantitative evaluation of thrombus composition11 and texture analysis of MRI-R2* maps can potentially estimate the clot content of red blood cell and iron12. Indeed, it is likely that neuroimaging studies on correlations with histological composition may contribute, in the future, to select patients for clinical trials on new targeted lytic therapies13.

 

Consistently with CT data, Clot Burden Score on admission T2*-MRI has been shown to significantly predict recanalization and 3-month outcome after intravenous thrombolysis14 and thrombus length predicted early recanalization after IVT in patients with minor stroke and large vessel occlusion15.

Thrombus characterisation by non-invasive neuroimaging provides transversal and clinically relevant data. Research should be boosted more than it has been since the description of hyperdense cerebral artery sign, 37 years ago. Indeed, imaging/histology correlations may have a role in driving personalized reperfusion strategies in the acute phase, significantly increasing their efficacy, and could also bring clues in routine practice to predict stroke etiology.

 

 

Acknowledgments: 

Dr Gregory Kuchcinski, Department of Neuroradiology, Lille University Hospital, France

Dr François Caparros, Department of Neurology, Stroke Unit, Lille University Hospital, France

 

 

References

 

  1. Gács G, Fox AJ, Barnett HJ, Vinuela F. CT visualization of intracranial arterial thromboembolism. Stroke. 1983;14:756–762.
  2. Leys D, Pruvo JP, Godefroy O, Rondepierre P, Leclerc X. Prevalence and significance of hyperdense middle cerebral artery in acute stroke. Stroke. 1992;23:317–324.
  3. Santos EMM, Marquering HA, den Blanken MD, Berkhemer OA, Boers AMM, Yoo AJ, et al. Thrombus Permeability Is Associated With Improved Functional Outcome and Recanalization in Patients With Ischemic Stroke. Stroke. 2016;47:732–741.
  4. Polito V, La Piana R, Del Pilar Cortes M, Tampieri D. Assessment of clot length with multiphase CT angiography in patients with acute ischemic stroke. Neuroradiol J. 2017;30:593–599.
  5. Yoo J, Baek J-H, Park H, Song D, Kim K, Hwang IG, et al. Thrombus Volume as a Predictor of Nonrecanalization After Intravenous Thrombolysis in Acute Stroke. Stroke. 2018;49:2108–2115.
  6. Puetz V, Dzialowski I, Hill MD, Subramaniam S, Sylaja PN, Krol A, et al. Intracranial thrombus extent predicts clinical outcome, final infarct size and hemorrhagic transformation in ischemic stroke: the clot burden score. Int J Stroke. 2008;3:230–236.
  7. Li G, Wu G, Qin Z, Li H, Cheng X, Cai Y. Prognostic Value of Clot Burden Score in Acute Ischemic Stroke after Reperfusion Therapies: A Systematic Review and Meta-Analysis. J Stroke Cerebrovasc Dis. 2019;28:104293.
  8. Baek J-H, Yoo J, Song D, Kim YD, Nam HS, Kim BM, et al. Predictive value of thrombus volume for recanalization in stent retriever thrombectomy. Sci Rep. 2017;7:15938.
  9. Riedel CH, 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.
  10. Bourcier R, Détraz L, Serfaty JM, Delasalle BG, Mirza M, Derraz I, et al. MRI Interscanner Agreement of the Association between the Susceptibility Vessel Sign and Histologic Composition of Thrombi. J Neuroimaging. 2017;27:577–582.
  11. Bourcier R, Pautre R, Mirza M, Castets C, Darcourt J, Labreuche J, et al. MRI Quantitative T2* Mapping to Predict Dominant Composition of In Vitro Thrombus. AJNR Am J Neuroradiol. 2019;40:59–64.
  12. Bretzner M, Lopes R, McCarthy R, Corseaux D, Auger F, Gunning G, et al. Texture parameters of R2* maps are correlated with iron concentration and red blood cells count in clot analogs: A 7-T micro-MRI study. J Neuroradiol. 2019;
  13. Janot K, Zhu F, Kerleroux B, Boulouis G, Shotar E, Premat K, et al. “Adaptative endovascular strategy to the CloT MRI in large intracranial vessel occlusion” (VECTOR): Study protocol of a randomized control trial. J Neuroradiol. 2019;
  14. Legrand L, Naggara O, Turc G, Mellerio C, Roca P, Calvet D, et al. Clot Burden Score on Admission T2*-MRI Predicts Recanalization in Acute Stroke. Stroke. 2013;44:1878–1884.
  15. Seners P, Delepierre J, Turc G, Henon H, Piotin M, Arquizan C, et al. Thrombus Length Predicts Lack of Post-Thrombolysis Early Recanalization in Minor Stroke With Large Vessel Occlusion. Stroke. 2019;50:761–764.

Tailoring specific interventions according to the type of thrombus: can neuroimaging help?

By Barbara Casolla, MD, PhD, Univ. Lille, Inserm U1171, Degenerative and Vascular Cognitive Disorders, CHU Lille, Department of Neurology, France
Twitter: @BarbaraCasolla

In 1983, Gács et al. reported the “hyperdense cerebral artery sign” as the earliest neuroimaging sign of acute ischemic stroke1, visible long before early ischemic parenchymal changes. This sign is present in about 40% of patients with a middle cerebral artery infarct, and it has a specificity of 100% and a sensibility of 30%2. Indeed, thrombus corresponds to higher local hematocrit level, due to extrusion of plasma from clotted cells within, explaining the increasing of Hounsfield unit (HU) on non-contrast computed tomography (CT).

Up-to-date, CT/CT-angiography(CTA) thrombus characterization has improved and brings hints for therapeutic choices and prognosis prediction. Indeed, beyond thrombus location, multiple other parameter related to thrombus characteristics, such as thrombus perviousness3, length4 and volume5, can be evaluated in the acute setting. The Clot Burden Score6, a CTA-based grading system has been successively developed, and reflects thrombus extent and location in the cerebral anterior circulation. Longer thrombus and more proximal location gained lower scores in this 10-point scoring system, and strongly predicted low successful recanalization rates and poor clinical outcome7–9.

Available data suggest that CT parameters can help decision strategies for reperfusion therapies: before starting mechanical thrombectomy, clot dimensions could allow planning the endovascular procedure with the appropriate size and length of stent retriever, increasing the rate of first-pass recanalization and obtaining higher likelihood of a favourable outcome8.

Moreover, clot histology predicts tissue plasminogen activator(rtPA)-mediated intravenous thrombolysis (IVT) resistance, with red blood cell-rich area being more drug permeable and rtPA susceptible. Susceptibility vessel sign (SVS) on T2* magnetic resonance imaging (MRI) and SusceptibilityWeighed Imaging (SWI) sequences is related to the presence of deoxyhemoglobin, which determines a strong paramagnetic effect determining a signal loss on T2*sequences (Figure).

Indeed, SVS presence seems to correlate with an RBC-dominant thrombus, with variable diagnostic accuracy10. Recently, thrombus T2* relaxation time (R2*) has been proposed as a method of quantitative evaluation of thrombus composition11 and texture analysis of MRI-R2* maps can potentially estimate the clot content of red blood cell and iron12. Indeed, it is likely that neuroimaging studies on correlations with histological composition may contribute, in the future, to select patients for clinical trials on new targeted lytic therapies13.

 

Consistently with CT data, Clot Burden Score on admission T2*-MRI has been shown to significantly predict recanalization and 3-month outcome after intravenous thrombolysis14 and thrombus length predicted early recanalization after IVT in patients with minor stroke and large vessel occlusion15.

Thrombus characterisation by non-invasive neuroimaging provides transversal and clinically relevant data. Research should be boosted more than it has been since the description of hyperdense cerebral artery sign, 37 years ago. Indeed, imaging/histology correlations may have a role in driving personalized reperfusion strategies in the acute phase, significantly increasing their efficacy, and could also bring clues in routine practice to predict stroke etiology.

 

 

Acknowledgments: 

Dr Gregory Kuchcinski, Department of Neuroradiology, Lille University Hospital, France

Dr François Caparros, Department of Neurology, Stroke Unit, Lille University Hospital, France

 

 

References

 

  1. Gács G, Fox AJ, Barnett HJ, Vinuela F. CT visualization of intracranial arterial thromboembolism. Stroke. 1983;14:756–762.
  2. Leys D, Pruvo JP, Godefroy O, Rondepierre P, Leclerc X. Prevalence and significance of hyperdense middle cerebral artery in acute stroke. Stroke. 1992;23:317–324.
  3. Santos EMM, Marquering HA, den Blanken MD, Berkhemer OA, Boers AMM, Yoo AJ, et al. Thrombus Permeability Is Associated With Improved Functional Outcome and Recanalization in Patients With Ischemic Stroke. Stroke. 2016;47:732–741.
  4. Polito V, La Piana R, Del Pilar Cortes M, Tampieri D. Assessment of clot length with multiphase CT angiography in patients with acute ischemic stroke. Neuroradiol J. 2017;30:593–599.
  5. Yoo J, Baek J-H, Park H, Song D, Kim K, Hwang IG, et al. Thrombus Volume as a Predictor of Nonrecanalization After Intravenous Thrombolysis in Acute Stroke. Stroke. 2018;49:2108–2115.
  6. Puetz V, Dzialowski I, Hill MD, Subramaniam S, Sylaja PN, Krol A, et al. Intracranial thrombus extent predicts clinical outcome, final infarct size and hemorrhagic transformation in ischemic stroke: the clot burden score. Int J Stroke. 2008;3:230–236.
  7. Li G, Wu G, Qin Z, Li H, Cheng X, Cai Y. Prognostic Value of Clot Burden Score in Acute Ischemic Stroke after Reperfusion Therapies: A Systematic Review and Meta-Analysis. J Stroke Cerebrovasc Dis. 2019;28:104293.
  8. Baek J-H, Yoo J, Song D, Kim YD, Nam HS, Kim BM, et al. Predictive value of thrombus volume for recanalization in stent retriever thrombectomy. Sci Rep. 2017;7:15938.
  9. Riedel CH, 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.
  10. Bourcier R, Détraz L, Serfaty JM, Delasalle BG, Mirza M, Derraz I, et al. MRI Interscanner Agreement of the Association between the Susceptibility Vessel Sign and Histologic Composition of Thrombi. J Neuroimaging. 2017;27:577–582.
  11. Bourcier R, Pautre R, Mirza M, Castets C, Darcourt J, Labreuche J, et al. MRI Quantitative T2* Mapping to Predict Dominant Composition of In Vitro Thrombus. AJNR Am J Neuroradiol. 2019;40:59–64.
  12. Bretzner M, Lopes R, McCarthy R, Corseaux D, Auger F, Gunning G, et al. Texture parameters of R2* maps are correlated with iron concentration and red blood cells count in clot analogs: A 7-T micro-MRI study. J Neuroradiol. 2019;
  13. Janot K, Zhu F, Kerleroux B, Boulouis G, Shotar E, Premat K, et al. “Adaptative endovascular strategy to the CloT MRI in large intracranial vessel occlusion” (VECTOR): Study protocol of a randomized control trial. J Neuroradiol. 2019;
  14. Legrand L, Naggara O, Turc G, Mellerio C, Roca P, Calvet D, et al. Clot Burden Score on Admission T2*-MRI Predicts Recanalization in Acute Stroke. Stroke. 2013;44:1878–1884.
  15. Seners P, Delepierre J, Turc G, Henon H, Piotin M, Arquizan C, et al. Thrombus Length Predicts Lack of Post-Thrombolysis Early Recanalization in Minor Stroke With Large Vessel Occlusion. Stroke. 2019;50:761–764.