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Common genetic variation indicates separate etiologies for periventricular and deep white matter hyperintensities

Nicola J Armstrong, Karen A Mather, Muralidharan Sargurupremraj, Maria J Knol, Rainer Malik, View ORCID ProfileClaudia L Satizabal, Lisa R Yanek, Wen Wei, Vilmundur Gudnason, Nicole D Deuker, Lloyd T Elliott, Edith Hofer, Neda Jahanshad, Shuo Li, Mark A Logue, Michelle Luciano, Markus Scholz, Albert Smith, Stella S Trompet, Dina Vojinovic, Rui Xia, Fidel Alfaro-Almagro, David Ames, Najaf Amin, Philippe Amouyel, Alexa S Beiser, Henry Brodaty, Ian J Deary, Christine Fennema-Notestine, Piyush G Gampwar, Rebecca Gottesman, Ludovica Griffanti, Clifford R Jack, Mark Jenkinson, Jiyang Jain, Brian G Kral, View ORCID ProfileJohn W Kwok, Leonie Lampe, David CM Liewald, Pauline Maillard, Jonathan Marchini, Mark E Bastin, Bernard Mazoyer, Lukas Pirpamer, José Rafael Romero, Gennady V Roshchupkin, View ORCID ProfilePeter R Schofield, Matthias L Schroeter, David J Stott, Anbupalam Thalamuth, Julian Trollor, Christophe Tzourio, Jeroen van der Grond, Meike W Vernooij, Veronica A Witte, Maragret J Wright, Qiong Yang, Moris Zoe, Siggi Siggurdsson, Arno Villringer, Helena Schmidt, Asta L Haberg, Cornelia M Van Duijn, J Wouter Jukema, Martin Dichigans, Ralph L Sacco, Clinton B Wright, William S Kremen, Lewis C Becker, Paul M Thompson, Lenore Launer, Thomas H Mosley, Joanna M Wardlaw, M Afran Ikram, Hieab HH Adams, Reinhold Schmidt, Stephen M Smith, Charles Decarli, Perminder S Sachdev, Myriam Fornage, Stephanie Debbette, Sudha Seshadri, Paul A Nyquist
doi: https://doi.org/10.1101/683367
Nicola J Armstrong
1Mathematics and Statistics, Murdoch University, Perth, Australia
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Karen A Mather
2Centre for Healthy Brain Ageing, School of Psychiatry, University of New South Wales, Sydney, Australia
3Neurosciences Research, School of Medical Sciences, University of New South Wales, Sydney Australia
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Muralidharan Sargurupremraj
4Univ. Bordeaux, Inserm, Bordeaux Population Health Research Center, Bordeaux, France
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Maria J Knol
5Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands
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Rainer Malik
6Institute for Stroke and Dementia Research (ISD), University Hospital, Ludwig-Maximilians-Universität LMU Munich, Germany
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Claudia L Satizabal
7Glenn Biggs Institute for Alzheimer’s & Neurodegenerative Diseases, UT Health San Antonio, San Antonio, TX, USA
8The Framingham Heart Study, Framingham, MA, USA
9Department of Neurology, Boston University School of Medicine, Boston, MA, USA
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Lisa R Yanek
10GeneSTAR Research Program, Johns Hopkins University School of Medicine, Baltimore, MD, USA
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Wen Wei
2Centre for Healthy Brain Ageing, School of Psychiatry, University of New South Wales, Sydney, Australia
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Vilmundur Gudnason
11Icelandic Heart Association, Kopavogur, Iceland
12University of Iceland, Reykjavik, Iceland
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Nicole D Deuker
13John P. Hussman Institute for Human Genomics, University of Miami, Miami, FL, USA
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Lloyd T Elliott
14Department of Statistics and Actuarial Science, Simon Fraser University, Burnaby, BC, Canada
15Wellcome Centre for Integrative Neuroimaging (WIN FMRIB), University of Oxford, Oxford, United Kingdom
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Edith Hofer
16Clinical Division of Neurogeriatrics, Department of Neurology, Medical University of Graz, Austria
17Institute for Medical Informatics, Statistics and Documentation, Medical University of Graz, Austria
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Neda Jahanshad
18Mark and Mary Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Marina del Rey, CA, USA
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Shuo Li
19Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA
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Mark A Logue
19Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA
20National Center for PTSD: Behavioral Science Division, VA Boston Healthcare System, Boston, MA, USA
21Department of Psychiatry and Biomedical Genetics Section, Boston University School of Medicine, Boston, MA, USA
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Michelle Luciano
22Centre for Cognitive Ageing and Cognitive Epidemiology, Psychology, University of Edinburgh, Edinburgh, UK
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Markus Scholz
23Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany
24LIFE Research Center for Civilization Disease, Leipzig, Germany
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Albert Smith
12University of Iceland, Reykjavik, Iceland
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Stella S Trompet
25Department of Internal Medicine, section of Gerontology and Geriatrics, Leiden University Medical Center, The Netherlands
26Department of Cardiology, Leiden University Medical Center, The Netherlands
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Dina Vojinovic
5Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands
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Rui Xia
27Brown Foundation Institute of Molecular Medicine, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, USA
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Fidel Alfaro-Almagro
15Wellcome Centre for Integrative Neuroimaging (WIN FMRIB), University of Oxford, Oxford, United Kingdom
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David Ames
28National Ageing Research Institute, Parkville, Victoria, Australia
29Academic Unit for Psychiatry of Old Age, University of Melbourne, St George’s Hospital, Kew, Australia
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Najaf Amin
5Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands
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Philippe Amouyel
30Lille University, Inserm, Institut Pasteur de Lille, RID-AGE - Risk factors and molecular determinants of aging-related diseases and Labex Distalz, Lille, France
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Alexa S Beiser
8The Framingham Heart Study, Framingham, MA, USA
9Department of Neurology, Boston University School of Medicine, Boston, MA, USA
19Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA
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Henry Brodaty
2Centre for Healthy Brain Ageing, School of Psychiatry, University of New South Wales, Sydney, Australia
31Dementia Centre for Research Collaboration, University of New South Wales, Sydney, Australia
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Ian J Deary
22Centre for Cognitive Ageing and Cognitive Epidemiology, Psychology, University of Edinburgh, Edinburgh, UK
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Christine Fennema-Notestine
32Department of Psychiatry, University of California, San Diego, La Jolla, CA, USA
33Center for Behavior Genetics of Aging, University of California, San Diego, La Jolla, CA, US
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Piyush G Gampwar
34Gottfried Schatz Research Center (for Cell Signaling, Metabolism and Aging), Medical University of Graz, Austria
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Rebecca Gottesman
35Department of Neurology, Cerebrovascular and stroke Division, Johns Hopkins University School of Medicine, Baltimore, MD, USA
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Ludovica Griffanti
15Wellcome Centre for Integrative Neuroimaging (WIN FMRIB), University of Oxford, Oxford, United Kingdom
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Clifford R Jack
36Department of Radiology, Mayo Clinic, Rochester, MN, USA
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Mark Jenkinson
15Wellcome Centre for Integrative Neuroimaging (WIN FMRIB), University of Oxford, Oxford, United Kingdom
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Jiyang Jain
2Centre for Healthy Brain Ageing, School of Psychiatry, University of New South Wales, Sydney, Australia
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Brian G Kral
10GeneSTAR Research Program, Johns Hopkins University School of Medicine, Baltimore, MD, USA
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John W Kwok
37Brain and Mind Centre - The University of Sydney, Camperdown, NSW, Australia
38School of Medical Sciences, University of New South Wales, Sydney, Australia
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Leonie Lampe
39Department of Neurology, Max-Planck-Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
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David CM Liewald
22Centre for Cognitive Ageing and Cognitive Epidemiology, Psychology, University of Edinburgh, Edinburgh, UK
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Pauline Maillard
40Imaging of Dementia and Aging (IDeA) Laboratory, Department of Neurology, University of California-Davis, Davis, CA, USA
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Jonathan Marchini
41Statistical Genetics and Methods at Regeneron Pharmaceuticals, Inc., New York, NY, USA
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Mark E Bastin
42Centre for Clinical Brain Sciences, University of Edinburgh & Brain Research Imaging Centre, University of Edinburgh, Edinburgh, United Kingdom
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Bernard Mazoyer
43Univ. Bordeaux, Institut des Maladies Neurodégénératives, Bordeaux, France
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Lukas Pirpamer
44Clinical Division of Neurogeriatrics, Department of Neurology, Medical University of Graz, Austria
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José Rafael Romero
8The Framingham Heart Study, Framingham, MA, USA
9Department of Neurology, Boston University School of Medicine, Boston, MA, USA
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Gennady V Roshchupkin
5Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands
45Department of Radiology and Nuclear Medicine, Erasmus MC, Rotterdam, the Netherlands
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Peter R Schofield
3Neurosciences Research, School of Medical Sciences, University of New South Wales, Sydney Australia
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Matthias L Schroeter
46Department of Neurology, Max-Planck-Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
47Day Clinic for Cognitive Neurology, University Hospital Leipzig, Leipzig, Germany
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David J Stott
48Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary and Life Sciences, University of Glasgow, United Kingdom
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Anbupalam Thalamuth
2Centre for Healthy Brain Ageing, School of Psychiatry, University of New South Wales, Sydney, Australia
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Julian Trollor
2Centre for Healthy Brain Ageing, School of Psychiatry, University of New South Wales, Sydney, Australia
49Department of Developmental Disability Neuropsychiatry, School of Psychiatry, University of New South Wales, Sydney, Australia
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Christophe Tzourio
4Univ. Bordeaux, Inserm, Bordeaux Population Health Research Center, Bordeaux, France
50CHU de Bordeaux, Public Health Department, Medical information Department, Bordeaux, France
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Jeroen van der Grond
51Department of Radiology, Leiden University Medical Center, The Netherlands
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Meike W Vernooij
5Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands
45Department of Radiology and Nuclear Medicine, Erasmus MC, Rotterdam, the Netherlands
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Veronica A Witte
39Department of Neurology, Max-Planck-Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
52Collaborative Research Center 1052 Obesity Mechanisms, Faculty of Medicine, University of Leipzig, Leipzig, Germany
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Maragret J Wright
53Queensland Brain Institute, The University of Queensland, St Lucia, QLD, Australia
54Centre for Advanced Imaging, The University of Queensland, St Lucia, QLD, Australia
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Qiong Yang
19Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA
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54Centre for Advanced Imaging, The University of Queensland, St Lucia, QLD, Australia
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Siggi Siggurdsson
11Icelandic Heart Association, Kopavogur, Iceland
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Arno Villringer
46Department of Neurology, Max-Planck-Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
47Day Clinic for Cognitive Neurology, University Hospital Leipzig, Leipzig, Germany
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Helena Schmidt
34Gottfried Schatz Research Center (for Cell Signaling, Metabolism and Aging), Medical University of Graz, Austria
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Asta L Haberg
55Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology, Trondheim, Norway
56Department of Radiology and Nuclear Medicine, Norwegian University of Science and Technology, Trondheim, Norway
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Cornelia M Van Duijn
5Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands
57Nuffield Department of Population Health, University of Oxford, Oxford, United Kingdom
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J Wouter Jukema
58Department of Cardiology, Leiden University Medical Center, The Netherlands
59Einthoven Laboratory for Experimental Vascular Medicine, LUMC, Leiden, the Netherlands
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Martin Dichigans
6Institute for Stroke and Dementia Research (ISD), University Hospital, Ludwig-Maximilians-Universität LMU Munich, Germany
60German Center for Neurodegenerative Diseases, Munich, Germany
61Munich Cluster for Systems Neurology (SyNergy), Munich, Germany
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Ralph L Sacco
62Dr. John T. Macdonald Foundation Department of Human Genetics, University of Miami, Miami, FL, USA
63Department of Public Health Sciences, Miller School of Medicine, University of Miami, Miami, FL USA
64Department of Neurology, Miller School of Medicine, University of Miami, Miami, FL USA
65Evelyn F. McKnight Brain Institute, Department of Neurology, University of Miami, Miami FL USA
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Clinton B Wright
66National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA
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William S Kremen
67Department of Psychiatry, University of California, San Diego, La Jolla, CA, USA
68Center for Behavior Genetics of Aging, University of California, San Diego, La Jolla, CA, USA
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Lewis C Becker
10GeneSTAR Research Program, Johns Hopkins University School of Medicine, Baltimore, MD, USA
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Paul M Thompson
69Mark and Mary Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Marina del Rey, CA, USA
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Lenore Launer
70Laboratory of Epidemiology and Population Sciences, National Institute on Aging, Intramural Research Program, National Institutes of Health, Bethesda, MD, USA
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Thomas H Mosley
71Departemnt of Geriatric Medicine, Memory Impairment and Neurodegenerative Dementia (MIND) Center, University of Mississippi Medical Center, Jackson, MS
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Joanna M Wardlaw
72Division of Neuroimaging Sciences, Brain Research Imaging Centre, University of Edinburgh. Edinburgh, UK
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M Afran Ikram
5Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands
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Hieab HH Adams
5Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands
45Department of Radiology and Nuclear Medicine, Erasmus MC, Rotterdam, the Netherlands
73Department of Clinical Genetics, Erasmus MC, Rotterdam, the Netherlands
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Reinhold Schmidt
16Clinical Division of Neurogeriatrics, Department of Neurology, Medical University of Graz, Austria
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Stephen M Smith
74Wellcome Centre for Integrative Neuroimaging (WIN FMRIB), University of Oxford, Oxford United Kingdom
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Charles Decarli
75Alzheimer’s Disease Center and Imaging of Dementia and Aging (IDeA) Laboratory, Department of Neurology and Center for Neuroscience University of California at Davis, Davis, CA USA
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Perminder S Sachdev
2Centre for Healthy Brain Ageing, School of Psychiatry, University of New South Wales, Sydney, Australia
76Neuropsychiatric Institute, Prince of Wales Hospital, Sydney, Australia
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Myriam Fornage
27Brown Foundation Institute of Molecular Medicine, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, USA
77Human Genetics Center, School of Public Health UT, Houston TX, USA
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Stephanie Debbette
4Univ. Bordeaux, Inserm, Bordeaux Population Health Research Center, Bordeaux, France
78CHU de Bordeaux (University Hospital), Department of Neurology, Bordeaux, France
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Sudha Seshadri
7Glenn Biggs Institute for Alzheimer’s & Neurodegenerative Diseases, UT Health San Antonio, San Antonio, TX, USA
8The Framingham Heart Study, Framingham, MA, USA
9Department of Neurology, Boston University School of Medicine, Boston, MA, USA
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Paul A Nyquist
10GeneSTAR Research Program, Johns Hopkins University School of Medicine, Baltimore, MD, USA
79Departments of Neurology, Critical Care Medicine, Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA
80Critical Care Medicine Department, National Institutes of Health, Bethesda MD, USA
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  • For correspondence: pnyquis1@jhmi.edu
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Abstract

We conducted a genome-wide association meta-analysis of two ischemic white matter disease subtypes in the brain, periventricular and deep white matter hyperintensities (PVWMH and DWMH). In 26,654 participants, we found 10 independent genome-wide significant loci only associated with PVWMH, four of which have not been described previously for total WMH burden (16q24.2, 17q21.31, 10q23.1, 7q36.1). Additionally, in both PVWMH and DWMH we observed the previous association of the 17q25.1 locus with total WMH. We found that both phenotypes have shared but also distinct genetic architectures, consistent with both different underlying and related pathophysiology. PVWMH had more extensive genetic overlap with small vessel ischemic stroke, and unique associations with several loci implicated in ischemic stroke. DWMH were characterized by associations with loci previously implicated in vascular as well as astrocytic and neuronal function. Our study confirms the utility of these phenotypes and identifies new candidate genes associated only with PVWMH.

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Common genetic variation indicates separate etiologies for periventricular and deep white matter hyperintensities
Nicola J Armstrong, Karen A Mather, Muralidharan Sargurupremraj, Maria J Knol, Rainer Malik, Claudia L Satizabal, Lisa R Yanek, Wen Wei, Vilmundur Gudnason, Nicole D Deuker, Lloyd T Elliott, Edith Hofer, Neda Jahanshad, Shuo Li, Mark A Logue, Michelle Luciano, Markus Scholz, Albert Smith, Stella S Trompet, Dina Vojinovic, Rui Xia, Fidel Alfaro-Almagro, David Ames, Najaf Amin, Philippe Amouyel, Alexa S Beiser, Henry Brodaty, Ian J Deary, Christine Fennema-Notestine, Piyush G Gampwar, Rebecca Gottesman, Ludovica Griffanti, Clifford R Jack, Mark Jenkinson, Jiyang Jain, Brian G Kral, John W Kwok, Leonie Lampe, David CM Liewald, Pauline Maillard, Jonathan Marchini, Mark E Bastin, Bernard Mazoyer, Lukas Pirpamer, José Rafael Romero, Gennady V Roshchupkin, Peter R Schofield, Matthias L Schroeter, David J Stott, Anbupalam Thalamuth, Julian Trollor, Christophe Tzourio, Jeroen van der Grond, Meike W Vernooij, Veronica A Witte, Maragret J Wright, Qiong Yang, Moris Zoe, Siggi Siggurdsson, Arno Villringer, Helena Schmidt, Asta L Haberg, Cornelia M Van Duijn, J Wouter Jukema, Martin Dichigans, Ralph L Sacco, Clinton B Wright, William S Kremen, Lewis C Becker, Paul M Thompson, Lenore Launer, Thomas H Mosley, Joanna M Wardlaw, M Afran Ikram, Hieab HH Adams, Reinhold Schmidt, Stephen M Smith, Charles Decarli, Perminder S Sachdev, Myriam Fornage, Stephanie Debbette, Sudha Seshadri, Paul A Nyquist
bioRxiv 683367; doi: https://doi.org/10.1101/683367
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Common genetic variation indicates separate etiologies for periventricular and deep white matter hyperintensities
Nicola J Armstrong, Karen A Mather, Muralidharan Sargurupremraj, Maria J Knol, Rainer Malik, Claudia L Satizabal, Lisa R Yanek, Wen Wei, Vilmundur Gudnason, Nicole D Deuker, Lloyd T Elliott, Edith Hofer, Neda Jahanshad, Shuo Li, Mark A Logue, Michelle Luciano, Markus Scholz, Albert Smith, Stella S Trompet, Dina Vojinovic, Rui Xia, Fidel Alfaro-Almagro, David Ames, Najaf Amin, Philippe Amouyel, Alexa S Beiser, Henry Brodaty, Ian J Deary, Christine Fennema-Notestine, Piyush G Gampwar, Rebecca Gottesman, Ludovica Griffanti, Clifford R Jack, Mark Jenkinson, Jiyang Jain, Brian G Kral, John W Kwok, Leonie Lampe, David CM Liewald, Pauline Maillard, Jonathan Marchini, Mark E Bastin, Bernard Mazoyer, Lukas Pirpamer, José Rafael Romero, Gennady V Roshchupkin, Peter R Schofield, Matthias L Schroeter, David J Stott, Anbupalam Thalamuth, Julian Trollor, Christophe Tzourio, Jeroen van der Grond, Meike W Vernooij, Veronica A Witte, Maragret J Wright, Qiong Yang, Moris Zoe, Siggi Siggurdsson, Arno Villringer, Helena Schmidt, Asta L Haberg, Cornelia M Van Duijn, J Wouter Jukema, Martin Dichigans, Ralph L Sacco, Clinton B Wright, William S Kremen, Lewis C Becker, Paul M Thompson, Lenore Launer, Thomas H Mosley, Joanna M Wardlaw, M Afran Ikram, Hieab HH Adams, Reinhold Schmidt, Stephen M Smith, Charles Decarli, Perminder S Sachdev, Myriam Fornage, Stephanie Debbette, Sudha Seshadri, Paul A Nyquist
bioRxiv 683367; doi: https://doi.org/10.1101/683367

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