Harmonizing brain magnetic resonance imaging methods for vascular contributions to neurodegeneration

Eric E Smith^{1

2

3}, Geert Jan Biessels⁴, François De Guio⁵, Frank Erik de Leeuw⁶, Simon Duchesne^{7

8}, Marco Düring^{9

10

11}, Richard Frayne^{1

2

3

12}, M Arfan Ikram¹³, Eric Jouvent⁵, Bradley J MacIntosh¹⁴, Michael J Thrippleton^{15

16

17}, Meike W Vernooij^{13

18}, Hieab Adams^{13

18}, Walter H Backes¹⁹, Lucia Ballerini^{15

16

17}, Sandra E Black^{20

21

22}, Christopher Chen²³, Rod Corriveau²⁴, Charles DeCarli²⁵, Steven M Greenberg²⁶, M Edip Gurol²⁶, Michael Ingrisch²⁷, Dominic Job^{15

16

17}, Bonnie Y K Lam²⁸, Lenore J Launer²⁹, Jennifer Linn³⁰, Cheryl R McCreary^{1

2

12}, Vincent C T Mok²⁸, Leonardo Pantoni³¹, G Bruce Pike^{1

2

3}, Joel Ramirez^{14

20}, Yael D Reijmer⁴, Jose Rafael Romero^{32

33}, Stefan Ropele³⁴, Natalia S Rost³⁵, Perminder S Sachdev³⁶, Christopher J M Scott^{14

20}, Sudha Seshadri³⁷, Mukul Sharma^{38

39}, Steven Sourbron⁴⁰, Rebecca M E Steketee¹⁸, Richard H Swartz^{41

42}, Robert van Oostenbrugge⁴³, Matthias van Osch⁴⁴, Sanneke van Rooden⁴⁵, Anand Viswanathan²⁶, David Werring⁴⁶, Martin Dichgans^{9

10

11}, Joanna M Wardlaw^{15

16

17}

Affiliations

¹ Department of Clinical Neurosciences, University of Calgary, Calgary, Alberta, Canada.
² Department of Radiology, University of Calgary, Calgary, Alberta, Canada.
³ Hotchkiss Brain Institute, University of Calgary, Alberta, Canada.
⁴ Department of Neurology, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, Netherlands.
⁵ Department of Neurology, Lariboisière Hospital, University Paris Diderot, Paris, France.
⁶ Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, Donders Center for Medical Neuroscience, Radboud University Medical Center, Nijmegen, Netherlands.
⁷ CERVO Research Center, Quebec Mental Health Institute, Québec, Canada.
⁸ Radiology Department, Université Laval, Québec, Canada.
⁹ Institute for Stroke and Dementia Research (ISD), University Hospital, Ludwig-Maximilians-Universität LMU, Munich, Germany.
¹⁰ German Center for Neurodegenerative Diseases (DZNE, Munich), Munich, Germany.
¹¹ Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.
¹² Seaman Family MR Centre, Foothills Medical Centre, Calgary, Alberta, Canada.
¹³ Department of Epidemiology, Erasmus University Medical Center, Rotterdam, Netherlands.
¹⁴ Heart and Stroke Foundation Canadian Partnership for Stroke Recovery, Department of Medical Biophysics, Sunnybrook Research Institute, University of Toronto, Ontario, Canada.
¹⁵ Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, UK.
¹⁶ Edinburgh Imaging, University of Edinburgh, Edinburgh, UK.
¹⁷ UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.
¹⁸ Department of Radiology and Nuclear Medicine, Erasmus University Medical Center, Rotterdam, The Netherlands.
¹⁹ Department of Radiology & Nuclear Medicine, School for Mental Health & Neuroscience, Maastricht University Medical Center, Maastricht, The Netherlands.
²⁰ Hurvitz Brain Sciences Research Program, Sunnybrook Research Institute, University of Toronto, Toronto, Ontario, Canada.
²¹ Heart and Stroke Foundation Canadian Partnership for Stroke Recovery, Toronto, Ontario, Canada.
²² Department of Medicine (Neurology), Sunnybrook Health Sciences Centre, University of Toronto, Toronto, Ontario, Canada.
²³ Memory Aging and Cognition Centre, Department of Pharmacology, National University of Singapore, Singapore.
²⁴ National Institute of Neurological Disorders and Stroke, Bethesda, MD, USA.
²⁵ Department of Neurology and Center for Neuroscience, University of California at Davis, Davis, CA, USA.
²⁶ J. Philip Kistler Stroke Research Center, Stroke Service and Memory Disorders Unit, Massachusetts General Hospital, Boston, MA, USA.
²⁷ Department of Radiology, Ludwig-Maximilians-University Hospital Munich, Munich, Germany.
²⁸ Therese Pei Fong Chow Research Centre for Prevention of Dementia, Gerald Choa Neuroscience Centre, Lui Che Woo Institute of Innovative Medicine, Department of Medicine and Therapeutics, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong.
²⁹ National Institute on Aging, National Institutes of Health, Bethesda, MD, USA.
³⁰ Institute of Neuroradiology, University Hospital Carl Gustav Carus, Dresden, Germany.
³¹ Luigi Sacco Department of Biomedical and Clinical Sciences, University of Milan, Milan, Italy.
³² Department of Neurology, Boston University School of Medicine, Boston, MA, USA.
³³ Framingham Heart Study, Framingham, MA, USA.
³⁴ Department of Neurology, Medical University of Graz, Graz, Austria.
³⁵ J. Philip Kistler Stroke Research Center, Massachusetts General Hospital, Boston, MA, USA.
³⁶ Centre for Healthy Brain Ageing, University of New South Wales, Sydney, Australia.
³⁷ Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases, University of Texas Health Sciences Center, San Antonio, TX, USA.
³⁸ Population Health Research Institute, Hamilton, Ontario, Canada.
³⁹ Department of Medicine (Neurology) McMaster University, Hamilton, Ontario, Canada.
⁴⁰ Imaging Biomarkers Group, Department of Biomedical Imaging Sciences, University of Leeds, Leeds, UK.
⁴¹ Department of Medicine (Neurology), University of Toronto, Toronto, Canada.
⁴² Hurvitz Brain Sciences Program, Sunnybrook Health Sciences Centre, University of Toronto, Toronto, Canada.
⁴³ Department of Neurology, School for Mental Health and Neuroscience, Maastricht University Medical Center, Maastricht, the Netherlands.
⁴⁴ C.J. Gorter Center for high field MRI, Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands.
⁴⁵ Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands.
⁴⁶ University College London Queen Square institute of Neurology, London, UK.

PMID: 30859119
PMCID: PMC6396326
DOI: 10.1016/j.dadm.2019.01.002

Review

Harmonizing brain magnetic resonance imaging methods for vascular contributions to neurodegeneration

Eric E Smith et al. Alzheimers Dement (Amst). 2019.

. 2019 Feb 26:11:191-204.

doi: 10.1016/j.dadm.2019.01.002. eCollection 2019 Dec.

Authors

Affiliations

¹ Department of Clinical Neurosciences, University of Calgary, Calgary, Alberta, Canada.
² Department of Radiology, University of Calgary, Calgary, Alberta, Canada.
³ Hotchkiss Brain Institute, University of Calgary, Alberta, Canada.
⁴ Department of Neurology, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, Netherlands.
⁵ Department of Neurology, Lariboisière Hospital, University Paris Diderot, Paris, France.
⁶ Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, Donders Center for Medical Neuroscience, Radboud University Medical Center, Nijmegen, Netherlands.
⁷ CERVO Research Center, Quebec Mental Health Institute, Québec, Canada.
⁸ Radiology Department, Université Laval, Québec, Canada.
⁹ Institute for Stroke and Dementia Research (ISD), University Hospital, Ludwig-Maximilians-Universität LMU, Munich, Germany.
¹⁰ German Center for Neurodegenerative Diseases (DZNE, Munich), Munich, Germany.
¹¹ Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.
¹² Seaman Family MR Centre, Foothills Medical Centre, Calgary, Alberta, Canada.
¹³ Department of Epidemiology, Erasmus University Medical Center, Rotterdam, Netherlands.
¹⁴ Heart and Stroke Foundation Canadian Partnership for Stroke Recovery, Department of Medical Biophysics, Sunnybrook Research Institute, University of Toronto, Ontario, Canada.
¹⁵ Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, UK.
¹⁶ Edinburgh Imaging, University of Edinburgh, Edinburgh, UK.
¹⁷ UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.
¹⁸ Department of Radiology and Nuclear Medicine, Erasmus University Medical Center, Rotterdam, The Netherlands.
¹⁹ Department of Radiology & Nuclear Medicine, School for Mental Health & Neuroscience, Maastricht University Medical Center, Maastricht, The Netherlands.
²⁰ Hurvitz Brain Sciences Research Program, Sunnybrook Research Institute, University of Toronto, Toronto, Ontario, Canada.
²¹ Heart and Stroke Foundation Canadian Partnership for Stroke Recovery, Toronto, Ontario, Canada.
²² Department of Medicine (Neurology), Sunnybrook Health Sciences Centre, University of Toronto, Toronto, Ontario, Canada.
²³ Memory Aging and Cognition Centre, Department of Pharmacology, National University of Singapore, Singapore.
²⁴ National Institute of Neurological Disorders and Stroke, Bethesda, MD, USA.
²⁵ Department of Neurology and Center for Neuroscience, University of California at Davis, Davis, CA, USA.
²⁶ J. Philip Kistler Stroke Research Center, Stroke Service and Memory Disorders Unit, Massachusetts General Hospital, Boston, MA, USA.
²⁷ Department of Radiology, Ludwig-Maximilians-University Hospital Munich, Munich, Germany.
²⁸ Therese Pei Fong Chow Research Centre for Prevention of Dementia, Gerald Choa Neuroscience Centre, Lui Che Woo Institute of Innovative Medicine, Department of Medicine and Therapeutics, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong.
²⁹ National Institute on Aging, National Institutes of Health, Bethesda, MD, USA.
³⁰ Institute of Neuroradiology, University Hospital Carl Gustav Carus, Dresden, Germany.
³¹ Luigi Sacco Department of Biomedical and Clinical Sciences, University of Milan, Milan, Italy.
³² Department of Neurology, Boston University School of Medicine, Boston, MA, USA.
³³ Framingham Heart Study, Framingham, MA, USA.
³⁴ Department of Neurology, Medical University of Graz, Graz, Austria.
³⁵ J. Philip Kistler Stroke Research Center, Massachusetts General Hospital, Boston, MA, USA.
³⁶ Centre for Healthy Brain Ageing, University of New South Wales, Sydney, Australia.
³⁷ Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases, University of Texas Health Sciences Center, San Antonio, TX, USA.
³⁸ Population Health Research Institute, Hamilton, Ontario, Canada.
³⁹ Department of Medicine (Neurology) McMaster University, Hamilton, Ontario, Canada.
⁴⁰ Imaging Biomarkers Group, Department of Biomedical Imaging Sciences, University of Leeds, Leeds, UK.
⁴¹ Department of Medicine (Neurology), University of Toronto, Toronto, Canada.
⁴² Hurvitz Brain Sciences Program, Sunnybrook Health Sciences Centre, University of Toronto, Toronto, Canada.
⁴³ Department of Neurology, School for Mental Health and Neuroscience, Maastricht University Medical Center, Maastricht, the Netherlands.
⁴⁴ C.J. Gorter Center for high field MRI, Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands.
⁴⁵ Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands.
⁴⁶ University College London Queen Square institute of Neurology, London, UK.

PMID: 30859119
PMCID: PMC6396326
DOI: 10.1016/j.dadm.2019.01.002

Abstract

Introduction: Many consequences of cerebrovascular disease are identifiable by magnetic resonance imaging (MRI), but variation in methods limits multicenter studies and pooling of data. The European Union Joint Program on Neurodegenerative Diseases (EU JPND) funded the HARmoNizing Brain Imaging MEthodS for VaScular Contributions to Neurodegeneration (HARNESS) initiative, with a focus on cerebral small vessel disease.

Methods: Surveys, teleconferences, and an in-person workshop were used to identify gaps in knowledge and to develop tools for harmonizing imaging and analysis.

Results: A framework for neuroimaging biomarker development was developed based on validating repeatability and reproducibility, biological principles, and feasibility of implementation. The status of current MRI biomarkers was reviewed. A website was created at www.harness-neuroimaging.org with acquisition protocols, a software database, rating scales and case report forms, and a deidentified MRI repository.

Conclusions: The HARNESS initiative provides resources to reduce variability in measurement in MRI studies of cerebral small vessel disease.

Keywords: Cerebrovascular disease; Dementia; Magnetic resonance imaging; Radiology; Stroke.

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Figures

**Fig. 1**
Imaging biomarker development framework for cerebral small vessel disease.

**Fig. 2**
Schematic overview of the neuroimaging biomarker development status for cerebral small vessel disease. The green light indicates validation data from two or more studies from independent research groups; yellow light indicates support from a single study or conflicting evidence from multiple studies; and red light indicates there is currently insufficient evidence. Abbreviations: WMH, white matter hyperintensities of presumed vascular origin; CMB, cerebral microbleeds; PVS, perivascular spaces; DTI, diffusion tensor imaging; BBB, blood-brain barrier. Proof of concept: evidence that the marker measures a specific change or process related to cerebral small vessel disease. Proof of principle/mechanism: evidence that the marker differs between patients with and without cerebral small vessel disease. Proof of effectiveness: evidence from larger scale multiple center studies that the marker differs between patients with and without cerebral small vessel disease. Repeatability: precision of repeated measurements under the same conditions using the same scanner. Reproducibility: replicate measurements on the same or similar objects (e.g., a phantom or human volunteers) in different locations using different scanners. Longitudinal: the rate of change over time has been defined. Monitoring: evidence that longitudinal changes in the marker are associated with progression of cerebral small vessel disease. Surrogate: evidence that changes in the marker are strongly associated with clinical outcomes in cerebral small vessel disease, such that changes in the marker could be considered a substitute for a clinical endpoint.

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References

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Harmonizing brain magnetic resonance imaging methods for vascular contributions to neurodegeneration

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Harmonizing brain magnetic resonance imaging methods for vascular contributions to neurodegeneration

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