Frontiers in Neuroscience (Aug 2022)
Deep profiling of multiple ischemic lesions in a large, multi-center cohort: Frequency, spatial distribution, and associations to clinical characteristics
- Anna K. Bonkhoff,
- Teresa Ullberg,
- Teresa Ullberg,
- Martin Bretzner,
- Martin Bretzner,
- Sungmin Hong,
- Markus D. Schirmer,
- Robert W. Regenhardt,
- Kathleen L. Donahue,
- Marco J. Nardin,
- Adrian V. Dalca,
- Adrian V. Dalca,
- Anne-Katrin Giese,
- Mark R. Etherton,
- Brandon L. Hancock,
- Steven J. T. Mocking,
- Elissa C. McIntosh,
- John Attia,
- John Attia,
- John W. Cole,
- Amanda Donatti,
- Christoph J. Griessenauer,
- Christoph J. Griessenauer,
- Laura Heitsch,
- Laura Heitsch,
- Lukas Holmegaard,
- Lukas Holmegaard,
- Katarina Jood,
- Katarina Jood,
- Jordi Jimenez-Conde,
- Jordi Jimenez-Conde,
- Steven J. Kittner,
- Robin Lemmens,
- Robin Lemmens,
- Christopher R. Levi,
- Christopher R. Levi,
- Caitrin W. McDonough,
- James F. Meschia,
- Chia-Ling Phuah,
- Stefan Ropele,
- Jonathan Rosand,
- Jonathan Rosand,
- Jonathan Rosand,
- Jaume Roquer,
- Jaume Roquer,
- Tatjana Rundek,
- Ralph L. Sacco,
- Reinhold Schmidt,
- Pankaj Sharma,
- Agnieszka Slowik,
- Alessandro Sousa,
- Tara M. Stanne,
- Daniel Strbian,
- Turgut Tatlisumak,
- Turgut Tatlisumak,
- Vincent Thijs,
- Vincent Thijs,
- Achala Vagal,
- Daniel Woo,
- Ramin Zand,
- Patrick F. McArdle,
- Bradford B. Worrall,
- Bradford B. Worrall,
- Christina Jern,
- Christina Jern,
- Arne G. Lindgren,
- Arne G. Lindgren,
- Jane Maguire,
- Ona Wu,
- Petrea Frid,
- Natalia S. Rost,
- Johan Wasselius,
- Johan Wasselius
Affiliations
- Anna K. Bonkhoff
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Teresa Ullberg
- Department of Clinical Sciences Lund, Radiology, Lund University, Lund, Sweden
- Teresa Ullberg
- Department of Radiology and Neuroradiology, Skåne University Hospital, Lund, Sweden
- Martin Bretzner
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Martin Bretzner
- U1171 – LilNCog (JPARC) – Lille Neurosciences Cognition and University of Lille, Inserm, CHU Lille, Lille, France
- Sungmin Hong
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Markus D. Schirmer
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Robert W. Regenhardt
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Kathleen L. Donahue
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Marco J. Nardin
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Adrian V. Dalca
- Computer Science and Artificial Intelligence Lab, Massachusetts Institute of Technology, Boston, MA, United States
- Adrian V. Dalca
- Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, United States
- Anne-Katrin Giese
- Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
- Mark R. Etherton
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Brandon L. Hancock
- Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, United States
- Steven J. T. Mocking
- Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, United States
- Elissa C. McIntosh
- Department of Psychiatry, Johns Hopkins School of Medicine, Baltimore, MD, United States
- John Attia
- Hunter Medical Research Institute, Newcastle, NSW, Australia
- John Attia
- 0School of Medicine and Public Health, University of Newcastle, Newcastle, NSW, Australia
- John W. Cole
- 1Department of Neurology, University of Maryland, School of Medicine and Veterans Affairs Maryland Health Care System, Baltimore, MD, United States
- Amanda Donatti
- 2School of Medical Sciences, The Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), University of Campinas (UNICAMP), Campinas, Brazil
- Christoph J. Griessenauer
- 3Department of Neurosurgery, Geisinger, Danville, PA, United States
- Christoph J. Griessenauer
- 4Department of Neurosurgery, Christian Doppler Clinic, Paracelsus Medical University, Salzburg, Austria
- Laura Heitsch
- 5Department of Emergency Medicine, Washington University School of Medicine, St. Louis, MO, United States
- Laura Heitsch
- 6Department of Neurology, Barnes-Jewish Hospital, Washington University School of Medicine, St. Louis, MO, United States
- Lukas Holmegaard
- 7Department of Clinical Neuroscience, Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Lukas Holmegaard
- 8Department of Neurology, Sahlgrenska University Hospital, Gothenburg, Sweden
- Katarina Jood
- 7Department of Clinical Neuroscience, Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Katarina Jood
- 8Department of Neurology, Sahlgrenska University Hospital, Gothenburg, Sweden
- Jordi Jimenez-Conde
- 9Department of Neurology, Neurovascular Research Group (NEUVAS), IMIM-Hospital del Mar (Institut Hospital del Mar d’Investigacions Mèdiques), Universitat Pompeu Fabra, Barcelona, Spain
- Jordi Jimenez-Conde
- 0Department of Medicine and Life Sciences (MELIS), Universitat Pompeu Fabra, Barcelona, Spain
- Steven J. Kittner
- 1Department of Neurology, University of Maryland, School of Medicine and Veterans Affairs Maryland Health Care System, Baltimore, MD, United States
- Robin Lemmens
- 1Department of Neurosciences, Experimental Neurology and Leuven Research Institute for Neuroscience, Disease (LIND), KU Leuven - University of Leuven, Leuven, Belgium
- Robin Lemmens
- 2Laboratory of Neurobiology, Department of Neurology, Vesalius Research Center (VIB), University Hospitals Leuven, Leuven, Belgium
- Christopher R. Levi
- 3Department of Neurology, John Hunter Hospital, Newcastle, NSW, Australia
- Christopher R. Levi
- 4Department of Pharmacotherapy, Translational Research, Center for Pharmacogenomics, University of Florida, Gainesville, FL, United States
- Caitrin W. McDonough
- 5Department of Neurology, Mayo Clinic, Jacksonville, FL, United States
- James F. Meschia
- 6Department of Neurology, Clinical Division of Neurogeriatrics, Medical University Graz, Graz, Austria
- Chia-Ling Phuah
- 6Department of Neurology, Barnes-Jewish Hospital, Washington University School of Medicine, St. Louis, MO, United States
- Stefan Ropele
- 7Henry and Allison McCance Center for Brain Health, Massachusetts General Hospital, Boston, MA, United States
- Jonathan Rosand
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Jonathan Rosand
- Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, United States
- Jonathan Rosand
- 8Department of Neurology, Evelyn F. McKnight Brain Institute, Miller School of Medicine, University of Miami, Miami, FL, United States
- Jaume Roquer
- 9Department of Neurology, Neurovascular Research Group (NEUVAS), IMIM-Hospital del Mar (Institut Hospital del Mar d’Investigacions Mèdiques), Universitat Pompeu Fabra, Barcelona, Spain
- Jaume Roquer
- 0Department of Medicine and Life Sciences (MELIS), Universitat Pompeu Fabra, Barcelona, Spain
- Tatjana Rundek
- 0School of Medicine and Public Health, University of Newcastle, Newcastle, NSW, Australia
- Ralph L. Sacco
- 0School of Medicine and Public Health, University of Newcastle, Newcastle, NSW, Australia
- Reinhold Schmidt
- 7Henry and Allison McCance Center for Brain Health, Massachusetts General Hospital, Boston, MA, United States
- Pankaj Sharma
- 9Institute of Cardiovascular Research, St Peter’s, Ashford Hospitals, Royal Holloway University of London (ICR2UL), Egham, United Kingdom
- Agnieszka Slowik
- 0Department of Neurology, Jagiellonian University Medical College, Kraków, Poland
- Alessandro Sousa
- 2School of Medical Sciences, The Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), University of Campinas (UNICAMP), Campinas, Brazil
- Tara M. Stanne
- 1Department of Laboratory Medicine, Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Daniel Strbian
- 2Department of Neurology, Helsinki University Hospital and University of Helsinki, Helsinki, Finland
- Turgut Tatlisumak
- 7Department of Clinical Neuroscience, Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Turgut Tatlisumak
- 8Department of Neurology, Sahlgrenska University Hospital, Gothenburg, Sweden
- Vincent Thijs
- 3Division of Stroke, Florey Institute of Neuroscience and Mental Health, Heidelberg, VIC, Australia
- Vincent Thijs
- 4Department of Neurology, Austin Health, Heidelberg, VIC, Australia
- Achala Vagal
- 5Department of Radiology, University of Cincinnati College of Medicine, Cincinnati, OH, United States
- Daniel Woo
- 6Department of Neurology, Rehabilitation Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, United States
- Ramin Zand
- 7Department of Neurology, Pennsylvania State University, Hershey, PA, United States
- Patrick F. McArdle
- 8Division of Endocrinology, Diabetes and Nutrition, Department of Medicine, University of Maryland School of Medicine, Baltimore, MD, United States
- Bradford B. Worrall
- 9Department of Neurology, University of Virginia, Charlottesville, VA, United States
- Bradford B. Worrall
- 0Department of Public Health Sciences, University of Virginia, Charlottesville, VA, United States
- Christina Jern
- 1Department of Laboratory Medicine, Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Christina Jern
- 1Department of Clinical Genetics and Genomics, Sahlgrenska University Hospital, Gothenburg, Sweden
- Arne G. Lindgren
- 2Department of Neurology, Skåne University Hospital, Lund, Sweden
- Arne G. Lindgren
- 3Department of Clinical Sciences Lund, Neurology, Lund University, Lund, Sweden
- Jane Maguire
- 4University of Technology, Faculty of Health, Sydney, NSW, Australia
- Ona Wu
- Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, United States
- Petrea Frid
- 3Department of Clinical Sciences Lund, Neurology, Lund University, Lund, Sweden
- Natalia S. Rost
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States
- Johan Wasselius
- Department of Clinical Sciences Lund, Radiology, Lund University, Lund, Sweden
- Johan Wasselius
- Department of Radiology and Neuroradiology, Skåne University Hospital, Lund, Sweden
- DOI
- https://doi.org/10.3389/fnins.2022.994458
- Journal volume & issue
-
Vol. 16
Abstract
Background purposeA substantial number of patients with acute ischemic stroke (AIS) experience multiple acute lesions (MAL). We here aimed to scrutinize MAL in a large radiologically deep-phenotyped cohort.Materials and methodsAnalyses relied upon imaging and clinical data from the international MRI-GENIE study. Imaging data comprised both Fluid-attenuated inversion recovery (FLAIR) for white matter hyperintensity (WMH) burden estimation and diffusion-weighted imaging (DWI) sequences for the assessment of acute stroke lesions. The initial step featured the systematic evaluation of occurrences of MAL within one and several vascular supply territories. Associations between MAL and important imaging and clinical characteristics were subsequently determined. The interaction effect between single and multiple lesion status and lesion volume was estimated by means of Bayesian hierarchical regression modeling for both stroke severity and functional outcome.ResultsWe analyzed 2,466 patients (age = 63.4 ± 14.8, 39% women), 49.7% of which presented with a single lesion. Another 37.4% experienced MAL in a single vascular territory, while 12.9% featured lesions in multiple vascular territories. Within most territories, MAL occurred as frequently as single lesions (ratio ∼1:1). Only the brainstem region comprised fewer patients with MAL (ratio 1:4). Patients with MAL presented with a significantly higher lesion volume and acute NIHSS (7.7 vs. 1.7 ml and 4 vs. 3, pFDR < 0.001). In contrast, patients with a single lesion were characterized by a significantly higher WMH burden (6.1 vs. 5.3 ml, pFDR = 0.048). Functional outcome did not differ significantly between patients with single versus multiple lesions. Bayesian analyses suggested that the association between lesion volume and stroke severity between single and multiple lesions was the same in case of anterior circulation stroke. In case of posterior circulation stroke, lesion volume was linked to a higher NIHSS only among those with MAL.ConclusionMultiple lesions, especially those within one vascular territory, occurred more frequently than previously reported. Overall, multiple lesions were distinctly linked to a higher acute stroke severity, a higher total DWI lesion volume and a lower WMH lesion volume. In posterior circulation stroke, lesion volume was linked to a higher stroke severity in multiple lesions only.
Keywords
- magnetic resonance imaging
- acute ischemic stroke
- lesion volume
- multiple acute ischemic lesions
- quantitative imaging
- Bayesian hierarchical regression