Quantitative MRI of the Spinal Cord

306 Pages·2014·46.155 MB·English

by  Julien Cohen-Adad and Claudia Wheeler-Kingshott (Eds.)

QUANTITATIVE
MRI OF THE
SPINAL CORD
EditedBy
J C -A
ULIEN OHEN DAD
InstituteofBiomedicalEngineering,PolytechniqueMontreal;FunctionalNeuroimagingUnit,
CRIUGM,Universite´deMontre´al,Montreal,QC,Canada
C A.M. W -K
LAUDIA HEELER INGSHOTT
NMRResearchUnit,DepartmentofNeuroinflammation,QueenSquareMSCentre,UCLInstituteofNeurology,
QueenSquare,London,UK
AMSTERDAM(cid:129)BOSTON(cid:129)HEIDELBERG(cid:129)LONDON
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SANFRANCISCO(cid:129)SINGAPORE(cid:129)SYDNEY(cid:129)TOKYO
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Dedication
Tomy parents,my sister and to Serge,
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Tomy family,
C.W.K
Preface
According to the legend, in about 250 AD, Saint quantitativetechniquesinthespinalcordwithcontribu-
Denis, the first bishop of Paris, had his head chopped tions frommany leadersin this research field.
off. He then picked up his head and walked about 10 What’sinthebook?Afterpresentinginsection1thema-
kilometers from Montmartre to his grave. There have jor clinical needs for quantitative markers of the spinal
been multiple reports of cephalophoria (from the greek cord, section 2 covers the hardware and technical chal-
ke´phaleˆ, head and phorein, carry), which is an episode lengesinherenttospinalcordimaging.Section3thenfo-
where a decapitated character gets up, picks up his cuses on structural quantitative techniques (diffusion,
head, and carries on walking. These stories suggest magnetization transfer, relaxation, atrophy measure-
a great deal about the role of the spinal cord, which is ments), section 4 on functional and vascular charac-
notsimplyarelaybetweenthebrainandtheperipheral terization, while section 5 is dedicated to metabolic
system,but isalso capableof generating complex func- measurementsusingmagneticresonancespectroscopy.
tional patterns, adapting and reorganizing itself. About Thepurposeofthisbookisclear:focusonthetechni-
1700 years later, magnetic resonance imaging (MRI) calaspectsofspinalcordMRIforaneasiertranslationto
made it possible to “see” the spinal cord from outside their clinical use. Description of cutting edge research
the body, providing new elements to elucidate the techniques as well as more established methods are
enigma of cephalophoria. included. Acquisition and analysis aspects arecovered.
Whythisbook?MRIofthespinalcordhastremendous The majority of the book contains technical details on
potential for improving diagnosis/prognosis in neuro- eachquantitativetechnique.However,itremainsacces-
degenerative diseases and trauma as well as for devel- sible for most researchers/clinicians familiar with MRI
oping and monitoring treatment strategies. In who wish to apply these techniques. Most existing
particular, quantitative techniques are being developed books on spinal cord MRI focus on qualitative rather
that provide a variety of imaging biomarkers sensitive than quantitative techniques used in clinical routine,
to tissue integrity and neuronal function. Although e.g.,T1/T2/PD-weightedMRI.Ourbookessentiallyfo-
most of these techniques have been validated and cuses on quantitative spinal cord MRI from a technical
appliedinthebrainoverthepast20years,quantitative point of view aiding adoption by a wider community.
spinalcordMRIisunderutilized,bothinresearchandin Moreover this textbook includes “cooking recipes”
the clinic, which is a direct consequence of the diffi- (wherever applicable) at the end of each section to
culties related to the numerous artifacts and low signal help researchers and clinicians implementing these
sensitivity that characterizes the spine region. Even methods in their practice. Tosummarize, this book:
though recent developments in a number of areas,
(cid:129) Introduces the theory behind each quantitative
including phased-array coils, acquisition protocols,
technique;
and processing techniques, helped improving and
(cid:129) Reviewstheir applicationsin the human spinal cord
sometimes overcoming some of the challenges, only
and describestheir pros/cons;
modesteffortshavebeendedicatedtomakethesedevel-
(cid:129) Proposesa simple protocolfor applying each
opments available to the broader community of re-
quantitativetechniqueto the spinal cord.
searchers and clinicians. To date, there is no consensus
on how to apply these techniques to the spinal cord. How did it start? Ironically,the idea ofeditinga book
Asaconsequence,onlyveryfewmultidisciplinarycen- on Quantitative MRI of the spinal cord first emerged dur-
ters around the world can benefit from state-of-the-art ing the international Human Brain Mapping conference,
quantitative techniques of the spinal cord. Although whichtookplacein2011inQuebecCity,Canada.During
thereareseveralbooksonquantitativeMRIofthebrain, this meeting, JCA organized a symposium on Diffusion
including the excellent book of Paul Tofts, there are andFunctionalMRIoftheSpinalCord:MethodsandClinical
none dedicated to quantitative MRI of the spinal cord. Application.Thissymposiumcaughttheattentionofthe
This gives the rationale for having a textbook that publisher,whoapproachedJCAwiththeideaofabook.
reviews and synthesizes recent scientific advances on CWK was one of the speakers and started discussing
xi
xii
PREFACE
withJCAtheneedfor suchabook,tryingtoencourage project. It is with great satisfaction and appreciation of
him to take on this challenge. Elsevier followed up the all contributors’ help that both editors, two years later,
initial discussion, contacted the editors, CWK and areproudofstatingthattheyhavesurvivedtheexperi-
JCA, who joined efforts to bring together this exciting ence by completing this book!
Contributors
KhaledAbdel-AzizDepartmentofBrainRepairandRehabil- Michael G. Fehlings Division of Neurosurgery, Department
itation, UCL Institute of Neurology, University College of Surgery, University of Toronto; Krembil Neuroscience
London,London,UK Center, Toronto Western Hospital, University Health
Daniel C. Alexander Centre for Medical Image Computing, Network, ON,Canada
Department of Computer Science, University College Massimo Filippi Institute of Experimental Neurology, Divi-
London,London,United Kingdom sion of Neuroscience, San Raffaele Scientific Institute,
Yaniv Assaf Department of Neurobiology, George S. Wise Vita-Salute SanRaffaele University, Milan,Italy
FacultyofLifeSciences,TelAvivUniversity,TelAviv,Israel Ju¨rgen Finsterbusch Department of Systems Neuroscience,
Walter H. Backes Department of Radiology, Maastricht Uni- University Medical Center Hamburg-Eppendorf,
Institut fu¨r Systemische Neurowissenschaften, Hamburg,
versity MedicalCenter,Maastricht, The Netherlands
Germany
Roland Bammer Center for Quantitative Neuroimaging,
Patrick Freund Spinal Cord Injury Center, University
Department of Radiology, Stanford University, Stanford,
Hospital Balgrist, University of Zu¨rich, Zu¨rich,
CA,USA
Switzerland
Robert L. Barry Vanderbilt University Institute of Imaging
John C. Gore Vanderbilt University Institute of Imaging
Science,VanderbiltUniversity,Nashville,TN,USA;Depart-
Science,VanderbiltUniversity,Nashville,TN,USA;Depart-
ment of Radiology and Radiological Sciences, Vanderbilt
ment of Radiology and Radiological Sciences, Vanderbilt
University, Nashville,TN, USA
University,Nashville,TN,USA;DepartmentofBiomedical
Jonathan C.W. Brooks Clinical Research Imaging Centre
Engineering, Vanderbilt University, Nashville, TN, USA;
(CRiCBristol), University ofBristol,Bristol, UK
DepartmentofPhysicsandAstronomy,VanderbiltUniver-
David W. Cadotte Division of Neurosurgery, Department of sity,Nashville, TN, USA
Surgery,UniversityofToronto;KrembilNeuroscienceCen-
Charles R.G. Guttmann Center for Neurological Imaging,
ter, TorontoWestern Hospital, University Health Network,
Brigham and Women’s Hospital, Harvard Medical School,
ON,Canada
Boston,MA, USA
Mara Cercignani Clinical Imaging Science Centre, Brighton
SamanthaJ.HoldsworthCenterforQuantitativeNeuroimag-
and Sussex Medical School, University of Sussex, Falmer,
ing, Department of Radiology, Stanford University,
EastSussex,UK
Stanford,CA, USA
Olga Ciccarelli Department of Brain Repair and Rehabilita-
Mark A. Horsfield Department of Cardiovascular Sciences,
tion, UCL Institute of Neurology, University College
University ofLeicester,Leicester,UK
London,London,UK
MinaKimDepartmentofDiagnosticRadiology,Universityof
JulienCohen-AdadInstitute ofBiomedicalEngineering, Pol-
HongKong, Hong Kong,China
ytechnique Montreal; Functional Neuroimaging Unit,
CRIUGM, Universite´ de Montre´al, Montreal, QC,Canada John Kramer Spinal Cord Injury Center, University Hospital
Balgrist, University ofZu¨rich, Zu¨rich, Switzerland
Armin Curt Spinal Cord Injury Center, University Hospital
Balgrist, University ofZu¨rich, Zu¨rich, Switzerland Cornelia Laule Radiology Department, and Pathology and
Laboratory Medicine Department, University of British
Enrico De Vita Lysholm Department of Neuroradiology,
Columbia, Vancouver,Canada
National Hospital for Neurology and Neurosurgery,
London, UK; Academic Neuroradiological Unit, Depart- Alex MacKay Radiology Department, and Physics and
ment of Brain Repair and Rehabilitation, Institute of Astronomy Department, University of British Columbia,
Neurology,University College London,London,UK Vancouver,Canada
RichardD.DortchVanderbiltUniversityInstituteofImaging Robbert J. Nijenhuis Department of Radiology, University
Science,VanderbiltUniversity,Nashville,TN,USA;Depart- MedicalCenterUtrecht,Utrecht, The Netherlands
ment of Radiology and Radiological Sciences, Vanderbilt Istvan PirkoDepartmentofNeurology,Mayo Clinic,College
University,Nashville,TN,USA;DepartmentofBiomedical ofMedicine, Rochester,MN, USA
Engineering, Vanderbilt University,Nashville, TN,USA Emine U. Saritas Department of Bioengineering, University
BenjaminM.EllingsonDepartmentofRadiologicalSciences, of California, Berkeley, CA, USA; Department of Electrical
DavidGeffenSchoolofMedicine,UniversityofCalifornia- and Electronics Engineering, Bilkent University, Ankara,
LosAngeles,LosAngeles, CA,USA Turkey
xiii
xiv
CONTRIBUTORS
Torben Schneider Department of Neuroinflammation, Paul E. Summers Department of Biomedical, Metabolic and
UCL Institute of Neurology, University College London, NeuralSciences,UniversityofModenaandReggioEmilia,
London,UK Modena, Italy; and Department of Radiology, European
Seth A. Smith Vanderbilt University Institute of Imaging Institute ofRadiology,Milan, Italy
Science,VanderbiltUniversity,Nashville,TN,USA;Depart- LawrenceL.WaldA.A.MartinosCenterforBiomedicalImag-
ment of Radiology and Radiological Sciences, Vanderbilt ing, Massachusetts General Hospital, Harvard Medical
University,Nashville,TN,USA;DepartmentofBiomedical School, Charlestown, MA, USA; Harvard-MIT Division of
Engineering, Vanderbilt University, Nashville, TN, USA; Health Sciences and Technology, MIT, Cambridge, MA,
DepartmentofPhysicsandAstronomy,VanderbiltUniver- USA
sity, Nashville, TN,USA Claudia A.M. Wheeler-Kingshott NMR Research Unit,
Bhavana S. Solanky NMR Research Unit, Department of Department of Neuroinflammation, Queen Square MS
Neuroinflammation, Institute of Neurology, University Centre, UCL Institute of Neurology, University College
College, London,UK London,London, UK
Acknowledgements
The editors are grateful to all the contributors for gratitudetoDr.SergeRossignol,whoindirectlyinitiated
accepting the daunting task of writing a chapter, their thisbookbyinoculatingmehispassion,knowledgeand
invaluablescientificcontribution,theirdiligence,profes- rigorous scientific method for the study of spinal cord.
sionalism and positive attitude throughout the whole Idedicatethis book to him.
process. The editors also thank the publishers, Mica CWK:IamreallygratefultoJCAforinvolvingmein
Haley for having initiated the first contact, and April theadventureofthisbook.IwishalsotothankGlen,my
Graham and Laura Jackson for her precious support husband, my children, Liam, Shane and Slade, all my
during the long path of edition. group, my colleagues, students and postdocs, who
JCA:IwouldliketothankCWKforbeingpartofthis sometimes have had to share my time with this book;
creation, it was a real pleasure to work on this exciting in particular, I’d like to thank Torben and Bhavana
project with her. I am indebted to all my teachers and who are also authors of two of the chapters. My grati-
mentors, notably Drs. Pierre Jannin, Habib Benali, tude goes definitely to Profs. David H Miller and Alan
Lawrence Wald, Bruce Rosen and Caterina Mainero as J Thompson who have supported me over the years
wellasmystudentsandformerandcurrentcolleagues, and who truly taught me the importance of spinal
Drs. Claudine Gauthier, Rick Hoge, Julien Doyon, cord involvement in disease, and Profs. Paul Tofts and
Fre´de´ric Lesage, Kawin Setsompop, Jonathan Polimeni, Gareth J Barker who were key in my formation and
Thomas Witzel, Boris Keil, Wei Zhao, Azma Mareyam, my understanding of how essential it is to develop
Jennifer McNab, Himanshu Bhat, Keith Heberlein, quantitativeMRItechniques.Butmyacknowledgments
Raphael Paquin, Christophe Grova and Pierre Bellec, can’t be complete without mentioning my colleagues
for their support, helpful discussions and pleasant and dearest friends, Drs. Olga Ciccarelli and Mara
time spent together. I wish also to thank my parents, Cercignani,withwhomIcontinuouslysharetheexcite-
my sister and my close friends, for their continuous ment (and struggles) of pushing MRI forward, in our
loveandsupport.Iwouldliketoexpressmyparticular joint effortof advancingmedicine.
xv
Introduction to “Quantitative MRI
of the Spinal Cord”
MRIisthemostversatiletechniquetostudythecen- are insufficient, certainly at 3 T. Quantitative MRI of
tralnervoussystemandprovidesawealthofbiochemi- the spine therefore is an extremely challenging
cal and biophysical information that supports the endeavor, requiring not only full understanding of the
diagnostic processes in a variety of neurological and quantitative MRI, but also a successful combat of spe-
psychiatric diseases. Unlike CT, not only the contrast cific spinal artifacts.
and information content in MRI can be manipulated in Thisbooktakesupthechallengetodiscussquantita-
aseeminglyendlessmannertohighlightanatomicalfea- tive MRI of the spinal cord and continues from where
turessuchasfiberorientation,butalsothephysiological the seminal textbook, Quantitative MRI of the Brain by
parameterssuchasperfusionandmetabolism,inanon- PaulToftsstops.Itdiscussesthetechnicalandclinicalis-
invasive fashion. The unprecedented opportunities to suesrelatedtoquantitativeMRIandprovidesthereader
quantifybraintissuepropertiesharborimportantinfor- insightintotheapplicationofthisversatiletechniquein
mation to unravel disease mechanisms for researchers its most challengingdyet clinically most meaningfuld
andprovide prognostic to patients. region. Being composed by experts around the globe
However,theadvantageofMRItodeterminequanti- who have devoted much of their time to master these
tativetissuepropertiesalsocomesatapricedtheresult- advanced techniques in such an eloquent area, this
inginformationisoftenhardtoquantifyunambiguously. volume depicts the biophysical background, technical
DifficultiestoquantifyMRIpropertiesinanaccurateand implementation, and clinical interpretation of quantita-
precisemannerreflectvariationinscannerperformance tiveMRIinthespinalcord.Forthosefrightenedtoapply
acrossspaceandtimeonagivenmachine,butcertainly these techniques, it even provides “cooking recipes”,
across scanners with variability in software and hard- advising how to implement such techniques success-
ware platforms. Even simple quantitativemeasures like fully and overcome the many hurdles that I have wit-
brainvolumeandrateofatrophyarepronetodifficulties nessed myself when trying to capitalize on the
instandardizingimagequalityandhamperimplementa- promises of MRI, which is such a delicate region, espe-
tion of quantitative MRI measures in daily practice or cially when trying to apply advanced pulse-sequences
eveninmulticenterresearchstudies. at highfield.
ThelevelofcomplexityincreaseswhenusingMRIto Withthesechallengesinmind,Itrustthereaderswill
study the spinal cord, an extremely relevant but rather appreciate the careful text of this volume edited by
smallstructure.Despiteitsundisputedclinicalrelevance Julien Cohen-Adad and Claudia Wheeler-Kingshott
todepictahostofpathologicalconditions,evenqualita- and gain access to the theoretical and practical knowl-
tive interpretation of spinalcordMRIisendangered by edgethatwillenablethemtocapitalizeonthepromises
additionaltechnicalcaveats,suchasincreasedsuscepti- of quantitativeMRIin such achallenging region.
bilityandpulsationartifacts.Anyradiologistcantestify
thatobtaininggoodqualityroutinespinalcordimaging Frederik Barkhof
is much more challenging than obtaining good quality ProfessorofNeuroradiology,Department ofRadiology,
brain MRI scans, and that manufacturer settings often VUUniversityMedicalCentre,Amsterdam,TheNetherlands.
xvii
C H A P T E R
1.1
Rationale for Quantitative MRI of the Human
Spinal Cord and Clinical Applications
Khaled Abdel-Aziz, Olga Ciccarelli
Department of Brain Repair and Rehabilitation, UCL Institute of Neurology, University College London, London, UK
1.1.1 INTRODUCTION The development of new quantitative MRI (qMRI)
techniques,whicharemoresensitivetochangeinunder-
Neuroaxonal injury of the spinal cord occurs in a lyingtissuemicrostructureandmetabolism,isproviding
broad spectrum of clinically and pathologically hetero- insights into the pathogenesis of a growing number of
geneous neurodegenerative diseases, typically with neurologicaldiseases,andisshowingpromiseforstudy-
serious clinical consequences for patients.1–4 Typically, ingpotentialbiomarkersofdiseaseprogression.
the clinical syndrome produced by injury to the spinal Thoughtfully designed mechanistic MRI studies can
cord includes weakness or paralysis of the limbs and complementhistopathologicalstudiesinunderstanding
trunk, with sensory disturbance and dysfunction of pathophysiologicalprocessesoccurringinvivo,helping
the gastrointestinal and genitourinary sphincters. The toidentifyimportantmediatorsofdiseaseandtherefore
spinal cord is therefore an important region of interest inform rational drug design. The insights gained from
for biomedical research. However, magnetic resonance recent studies into cellular and pathophysiological ab-
imaging (MRI) of the spinal cord is more challenging normalities in multiple sclerosis (MS) have aided our
than that of the brain due to the smaller cross- understanding of the disease and may be valuable in
sectional area of the spinal cord, motion artifacts future therapeutic trials of neuroprotective agents.8 It
from cerebrospinal fluid (CSF) flow with each cardiac is predicted that qMRI will play an important role in
and respiratory cycle, and susceptibility to artifacts drug trials, since qMRI-derived measures can be used
from surrounding tissues.5–7 Advances in neuroimag- as biomarkers of disease progression and to monitor
ing techniques and postprocessing have allowed prog- treatment response. In addition, it is anticipated that
ress to be made in recent years, with a subsequent rise qMRImightbeusedtoriskstratifyandcharacterizepa-
in the number of studies investigating spinal cord tients on entry into trials. A recent study showing that
diseases using MRI. longitudinal changes in whole-brain and tract-specific
diffusiontensorimaging(DTI)indicesandthemagneti-
zation transfer ratio (MTR) can be reliably quantified,
WHAT IS QUANTITATIVE suggestingthat clinicaltrialsusing theseoutcome mea-
MRI (qMRI)? suresarefeasible.9Whilesimilar,longitudinalstudiesin
patientswithspinalcorddiseasesarecurrentlylacking,
As opposed to structural MRI (e.g., T1- or
thiswillnodoubtbethefocusoffuturework.Infact,itis
T2-weighted imaging), quantitative MRI (qMRI) aims
essential that reliable imaging biomarkers of the spinal
at providing values that are intrinsic to the tissue
cord are validated to prepare us for the emergence of
properties.qMRIhastheadvantageofprovidingab-
neuroprotectivedrugs.
solute and normative values that could be used for
This chapter will briefly review the qMRI techniques
diagnosis, prognosis, multiple-site studies, and
mostcommonlyappliedtothespinalcord,andthenfocus
ultimatelyclinicaltrials.
on reviewing data from qMRI studies in patients with
neurodegenerative spinal cord disease, and in animal
QuantitativeMRIoftheSpinalCord
http://dx.doi.org/10.1016/B978-0-12-396973-6.00001-0 3 Copyright(cid:1)2014ElsevierInc.Allrightsreserved.