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March 08, 2022; 98 (10) Research Article

Cerebral Microbleeds and Acute Hematoma Characteristics in the ATACH-2 and MISTIE III Trials

View ORCID ProfileJessica R. Magid-Bernstein, Yunke Li, Sung-Min Cho, Pirouz J. Piran, David J. Roh, Ajay Gupta, Ashkan Shoamanesh, Alexander Merkler, Cenai Zhang, Radhika Avadhani, Nataly Montano, Constantino Iadecola, Guido J. Falcone, Kevin N. Sheth, Adnan I. Qureshi, Jonathan Rosand, Joshua Goldstein, Issam Awad, Daniel F. Hanley, Hooman Kamel, Wendy C. Ziai, Santosh B. Murthy
First published December 22, 2021, DOI: https://doi.org/10.1212/WNL.0000000000013247
Jessica R. Magid-Bernstein
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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  • ORCID record for Jessica R. Magid-Bernstein
Yunke Li
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Sung-Min Cho
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Pirouz J. Piran
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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David J. Roh
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Ajay Gupta
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Ashkan Shoamanesh
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Alexander Merkler
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Cenai Zhang
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Radhika Avadhani
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Nataly Montano
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Constantino Iadecola
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Guido J. Falcone
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Kevin N. Sheth
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Adnan I. Qureshi
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Jonathan Rosand
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Joshua Goldstein
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Issam Awad
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Daniel F. Hanley
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Hooman Kamel
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Wendy C. Ziai
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Santosh B. Murthy
From the Division of Neurocritical Care and Emergency Neurology (J.R.M.-B., A.M., C.Z., C.I., H.K., S.B.M.), Department of Neurology, Yale University School of Medicine, New Haven, CT; Brain Injury Outcomes Center (Y.L., R.A., N.M., D.H.), Johns Hopkins University; Division of Neurosciences Critical Care (S.-M.C., P.J.P., W.C.Z.), Johns Hopkins University School of Medicine, Baltimore, MD; Vagelos College of Physicians and Surgeons (D.J.R.), Department of Neurology, Columbia University; Department of Radiology (A.G.), Clinical and Translational Neuroscience Unit (G.F., K.S.), Feil Family Brain and Mind Research Institute, and Department of Neurology (G.F., K.S.), Weill Cornell Medicine, New York, NY; Department of Neurology (A.S.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; Zeenat Qureshi Stroke Institutes (A.Q.) and Department of Neurology (A.Q.), University of Missouri, Columbia; Henry and Allison McCance Center for Brain Health (J.R.), Hemorrhagic Stroke Research Program (J.R.), J. Philip Kistler Stroke Research Center, and Department of Emergency Medicine (J.G.), Massachusetts General Hospital, Boston; and Department of Neurological Surgery (I.A.), University of Chicago School of Medicine, IL. Yunke Li is currently at The George Institute China at Peking University Health Sciences Center, Beijing, China.
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Cerebral Microbleeds and Acute Hematoma Characteristics in the ATACH-2 and MISTIE III Trials
Jessica R. Magid-Bernstein, Yunke Li, Sung-Min Cho, Pirouz J. Piran, David J. Roh, Ajay Gupta, Ashkan Shoamanesh, Alexander Merkler, Cenai Zhang, Radhika Avadhani, Nataly Montano, Constantino Iadecola, Guido J. Falcone, Kevin N. Sheth, Adnan I. Qureshi, Jonathan Rosand, Joshua Goldstein, Issam Awad, Daniel F. Hanley, Hooman Kamel, Wendy C. Ziai, Santosh B. Murthy
Neurology Mar 2022, 98 (10) e1013-e1020; DOI: 10.1212/WNL.0000000000013247

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Abstract

Background and Objectives To study the relationship between the presence of cerebral microbleeds (CMBs) and acute hematoma characteristics among patients with primary intracerebral hemorrhage (ICH).

Methods We pooled individual patient data from the Antihypertensive Treatment of Acute Cerebral Hemorrhage 2 (ATACH-2) trial and the Minimally Invasive Surgery Plus Alteplase for Intracerebral Hemorrhage Evacuation phase 3 (MISTIE III) trial. We included individuals with a brain MRI scan. Exposure was the presence of a CMB. The coprimary outcomes were admission ICH volume and hematoma expansion. Mixed-effects linear and logistic regression models were used, with demographics and comorbid conditions considered fixed effects and the study cohort treated as a random effect. Additional analyses assessed the relationship between CMB topography and number and hematoma characteristics.

Results Of the 1,499 patients with ICH enrolled in the parent trials, 466 (31.1%) were included in this analysis, and 231 (49.6%) patients had CMBs. In adjusted models, presence of CMBs was associated with smaller ICH volume (β = −0.26, 95% confidence interval [CI] −0.44 to −0.08) and lower odds of hematoma expansion (odds ratio 0.65, 95% CI 0.40–0.95; p = 0.04). The strength of association between CMBs and hematoma characteristics increased with increasing number of CMBs. The location of the CMBs and the severity of leukoaraiosis did not modify these results.

Discussion In a pooled cohort of patients with ICH, our results are consistent with the hypothesis that more severe underlying small vessel disease, as represented by CMBs, leads to smaller baseline hematoma volumes and reduced hematoma expansion. Underlying cerebral small vessel disease may be of prognostic significance after ICH.

Trial Registration Information ClinicalTrials.gov Identifier: NCT01176565 and NCT01827046.

Classification of Evidence This study provides Class II evidence that the presence of microbleeds on MRI is associated with a smaller ICH volume at presentation and a lower rate of hematoma expansion on follow-up imaging.

Glossary

ATACH-2=
Antihypertensive Treatment of Acute Cerebral Hemorrhage 2;
CI=
confidence interval;
CMB=
cerebral microbleed;
CSVD=
cerebral small vessel disease;
ICH=
intracerebral hemorrhage;
MISTIE III=
Minimally Invasive Surgery Plus Alteplase for Intracerebral Hemorrhage Evacuation phase 3;
OR=
odds ratio;
WMH=
white matter hyperintensities

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • ↵* These authors contributed equally to this work.

  • Class of Evidence: NPub.org/coe

  • Received May 10, 2021.
  • Accepted in final form December 13, 2021.
  • © 2021 American Academy of Neurology
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