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Neuroimaging standards for research into small vessel disease—advances since 2013 - 22/06/23

Doi : 10.1016/S1474-4422(23)00131-X 
Marco Duering, ProfMD a, b, c, , , Geert Jan Biessels, ProfPhD d, Amy Brodtmann, ProfPhD f, g, Christopher Chen, FRCP h, i, Charlotte Cordonnier, ProfPhD j, Frank-Erik de Leeuw, ProfPhD k, Stéphanie Debette, ProfPhD l, s, Richard Frayne, PhD m, o, p, q, Eric Jouvent, ProfMD t, u, Natalia S Rost, ProfMD v, Annemieke ter Telgte, PhD y, Rustam Al-Shahi Salman, ProfPhD z, Walter H Backes, ProfPhD ac, ad, ae, Hee-Joon Bae, MD ag, ah, Rosalind Brown, PhD z, aa, Hugues Chabriat, ProfMD ai, Alberto De Luca, PhD e, Charles deCarli, ProfMD aj, Anna Dewenter, MSc a, Fergus N Doubal, PhD z, Michael Ewers, ProfPhD a, Thalia S Field, MD ak, al, Aravind Ganesh, PhD m, n, p, r, Steven Greenberg, ProfPhD v, Karl G Helmer, PhD w, x, am, Saima Hilal, PhD an, Angela C C Jochems, MSc z, aa, Hanna Jokinen, PhD ao, ap, Hugo Kuijf, PhD e, Bonnie Y K Lam, PhD aq, ar, as, at, au, av, aw, ax, Jessica Lebenberg, PhD t, u, Bradley J MacIntosh, PhD ay, az, ba, Pauline Maillard, PhD aj, Vincent C T Mok, ProfMD aq, ar, as, at, au, av, aw, Leonardo Pantoni, ProfMD bb, Salvatore Rudilosso, PhD bc, Claudia L Satizabal, PhD bd, be, bf, bg, Markus D Schirmer, PhD v, Reinhold Schmidt, ProfMD bh, Colin Smith, ProfMD z, Julie Staals, PhD ad, af, Michael J Thrippleton, PhD z, ab, Susanne J van Veluw, PhD v, Prashanthi Vemuri, ProfPhD bi, Yilong Wang, ProfPhD bj, David Werring, ProfPhD bk, Marialuisa Zedde, MD bl, Rufus O Akinyemi, ProfPhD bm, Oscar H Del Brutto, ProfMD bn, Hugh S Markus, ProfMD bo, Yi-Cheng Zhu, ProfMD bp, Eric E Smith, ProfMD m, n, o, p, , Martin Dichgans, ProfMD a, bq, br, bs, , Joanna M Wardlaw, ProfMD z, aa, ,
a Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Munich, Germany 
b Medical Image Analysis Center, University of Basel, Basel, Switzerland 
c Department of Biomedical Engineering, University of Basel, Basel, Switzerland 
d Department of Neurology, University Medical Center Utrecht, Utrecht, Netherlands 
e Image Sciences Institute, UMC Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands 
f Cognitive Health Initiative, Central Clinical School, Monash University, Melbourne, VIC, Australia 
g Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, VIC, Australia 
h Department of Pharmacology, Memory Aging and Cognition Centre, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 
i Department of Psychological Medicine, Memory Aging and Cognition Centre, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 
j Université de Lille, INSERM, CHU Lille, U1172—Lille Neuroscience and Cognition (LilNCog), Lille, France 
k Department of Neurology, Donders Center for Medical Neuroscience, Radboudumc, Nijmegen, Netherlands 
l Bordeaux Population Health Research Center, University of Bordeaux, INSERM, UMR 1219, Bordeaux, France 
m Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada 
n Department of Community Health Sciences, University of Calgary, Calgary, AB, Canada 
o Department of Radiology, University of Calgary, Calgary, AB, Canada 
p Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada 
q Seaman Family MR Research Centre, Foothills Medical Centre, University of Calgary, Calgary, AB, Canada 
r Mathison Centre for Mental Health Research and Education, University of Calgary, Calgary, AB, Canada 
s Department of Neurology, Institute for Neurodegenerative Diseases, CHU de Bordeaux, Bordeaux, France 
t AP-HP, Lariboisière Hospital, Translational Neurovascular Centre, FHU NeuroVasc, Université Paris Cité, Paris, France 
u Université Paris Cité, INSERM UMR 1141, NeuroDiderot, Paris, France 
v Department of Neurology, Massachusetts General Hospital, Boston, MA, USA 
w Department of Radiology, Massachusetts General Hospital, Boston, MA, USA 
x Athinoula A Martinos Center for Biomedical Imaging, Boston, MA, USA 
y VASCage—Research Centre on Vascular Ageing and Stroke, Innsbruck, Austria 
z Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, UK 
aa UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK 
ab Edinburgh Imaging and Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, UK 
ac School for Mental Health and Neuroscience, Maastricht University Medical Center, Maastricht, Netherlands 
ad School for Cardiovascular Diseases, Maastricht University Medical Center, Maastricht, Netherlands 
ae Department of Radiology and Nuclear Medicine, Maastricht University Medical Center, Maastricht, Netherlands 
af Department of Neurology, Maastricht University Medical Center, Maastricht, Netherlands 
ag Department of Neurology, Seoul National University College of Medicine, Seoul, South Korea 
ah Cerebrovascular Disease Center, Seoul National University Bundang Hospital, Seongn-si, South Korea 
ai Centre Neurovasculaire Translationnel, CERVCO, INSERM U1141, FHU NeuroVasc, Université Paris Cité, Paris, France 
aj Department of Neurology and Center for Neuroscience, University of California, Davis, CA, USA 
ak Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, BC, Canada 
al Vancouver Stroke Program, Division of Neurology, University of British Columbia, Vancouver, BC, Canada 
am Department of Radiology, Harvard Medical School, Boston, MA, USA 
an Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore 
ao Division of Neuropsychology, HUS Neurocenter, Helsinki University Hospital, University of Helsinki, Helsinki, Finland 
ap Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki, Finland 
aq Division of Neurology, Department of Medicine and Therapeutics, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China 
ar Gerald Choa Neuroscience Institute, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China 
as Margaret KL Cheung Research Centre for Management of Parkinsonism, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China 
at Therese Pei Fong Chow Research Centre for Prevention of Dementia, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China 
au Lui Che Woo Institute of Innovative Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China 
av Li Ka Shing Institute of Health Science, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China 
aw Lau Tat-chuen Research Centre of Brain Degenerative Diseases in Chinese, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China 
ax Nuffield Department of Clinical Neurosciences, Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UK 
ay Sandra E Black Centre for Brain Resilience and Repair, Hurvitz Brain Sciences, Physical Sciences Platform, Sunnybrook Research Institute, Toronto, ON, Canada 
az Department of Medical Biophysics, University of Toronto, Toronto, ON, Canada 
ba Computational Radiology and Artificial Intelligence Unit, Radiology and Nuclear Medicine, Oslo University Hospital, Oslo, Norway 
bb Department of Biomedical and Clinical Science, University of Milan, Milan, Italy 
bc Comprehensive Stroke Center, Department of Neuroscience, Hospital Clinic and August Pi i Sunyer Biomedical Research Institute (IDIBAPS), Barcelona, Spain 
bd Glenn Biggs Institute for Alzheimer’s and Neurodegenerative Diseases, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA 
be Department of Population Health Sciences, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA 
bf Department of Neurology, Boston University Medical Center, Boston, MA, USA 
bg Framingham Heart Study, Framingham, MA, USA 
bh Department of Neurology, Medical University Graz, Graz, Austria 
bi Mayo Clinic, Department of Radiology, Rochester, MN, USA 
bj Beijing Tiantan Hospital, Capital Medical University, Beijing, China 
bk Stroke Research Centre, UCL Queen Square Institute of Neurology, London, UK 
bl Neurology Unit, Stroke Unit, Department of Neuromotor Physiology and Rehabilitation, Azienda Unità Sanitaria-IRCCS di Reggio Emilia, Reggio Emilia, Italy 
bm Neuroscience and Ageing Research Unit, Institute for Advanced Medical Research and Training, College of Medicine, University of Ibadan, Ibadan, Nigeria 
bn School of Medicine and Research Center, Universidad de Especialidades Espiritu Santo, Ecuador 
bo Stroke Research Group, Department of Clinical Neuroscience, University of Cambridge, Cambridge, UK 
bp Department of Neurology, Peking Union Medical College Hospital, Beijing, China 
bq Munich Cluster for Systems Neurology (SyNergy), Munich, Germany 
br German Center for Neurodegenerative Diseases (DZNE), Munich, Germany 
bs German Centre for Cardiovascular Research (DZHK), Munich, Germany 

* Correspondence to: Prof Joanna M Wardlaw, Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK Centre for Clinical Brain Sciences University of Edinburgh Edinburgh EH16 4SB UK ** Prof Marco Duering, Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Munich 81377, Germany Institute for Stroke and Dementia Research (ISD) University Hospital LMU Munich Munich 81377 Germany

Summary

Cerebral small vessel disease (SVD) is common during ageing and can present as stroke, cognitive decline, neurobehavioural symptoms, or functional impairment. SVD frequently coexists with neurodegenerative disease, and can exacerbate cognitive and other symptoms and affect activities of daily living. Standards for Reporting Vascular Changes on Neuroimaging 1 (STRIVE-1) categorised and standardised the diverse features of SVD that are visible on structural MRI. Since then, new information on these established SVD markers and novel MRI sequences and imaging features have emerged. As the effect of combined SVD imaging features becomes clearer, a key role for quantitative imaging biomarkers to determine sub-visible tissue damage, subtle abnormalities visible at high-field strength MRI, and lesion-symptom patterns, is also apparent. Together with rapidly emerging machine learning methods, these metrics can more comprehensively capture the effect of SVD on the brain than the structural MRI features alone and serve as intermediary outcomes in clinical trials and future routine practice. Using a similar approach to that adopted in STRIVE-1, we updated the guidance on neuroimaging of vascular changes in studies of ageing and neurodegeneration to create STRIVE-2.

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