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NUCLEUS PULPOSUS DEFORMATION
IN RESPONSE TO LUMBAR SPINE TORSION
Peter J. Fazey
B.App.Sc. (PT), Grad.Dip.Manip.Ther. (Curtin), FACP
Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy
July 2011
The Centre for Musculoskeletal Studies
School of Surgery
The University of Western Australia
ABSTRACT
Page i
Background
The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus
(AF) and the proteoglycan based, hydrophilic nucleus pulposus (NP). The primary role
of the NP is load attenuation which it achieves by deforming within the confines of the
anulus via a hydrostatic mechanism. The pattern of deformation is assumed to be away
from the position of offset loading. Changes in spinal posture result in variable loading.
Sagittal plane positioning has been shown to result in deformation of the NP towards
the convexity in most cases. Primary uniplanar lumbar segment movement results in
additional movement in a secondary plane. Spinal rotation, though small in range
intersegmentally, plays an important role in locomotion and contributes to multiplanar
motion and spinal flexibility. Rotation is also implicated as a common mechanism by
which the IVD may be injured. Few data exist reporting the direction of NP deformation
relative to rotated positions. Such information may inform the knowledge base on
injuring mechanisms and normal lumbar spine mechanics.
Purpose
The primary purpose of this thesis investigation was to quantify the in vivo effect of
rotation postures on lumbar NP deformation and to report the predictability of the
direction of that deformation. Additionally, the effects of coincident coronal plane
positions, age related changes and spinal deformity (scoliosis) were examined to
determine the relative influences of such factors on the internal mechanism of the IVD.
The principal hypothesis was that the NP would deform in all cases and conditions in a
predictable direction and with a magnitude proportional to the resultant segmental
angulation.
Methods
This investigation is divided into two main themes. The first describes the development
of a reliable methodology and reports normative data for NP deformation; the second
applies the methodology to subject populations with age changes in the IVD and
idiopathic scoliosis with a secondary lumbar curve. An initial ex vivo Computerised
Tomography (CT) based study examined the influence of joint morphology and IVD
degeneration on intersegmental rotation ranges. Three human osteoligamentous lumbar
Page ii
spines were placed in a purpose built torsion apparatus. Following application of axial
plane loading, displacements were tracked using a three dimensional motion analysis
instrument [Polhemius, Burlington, USA]. CT scanning was performed at incremental
loads and subsequently analysed for segmental rotation range and zygapophysial joint
gapping relative to disc pathology.
This study raised the question of the effect of rotation on IVD mechanics. Subsequently
a novel series of in vivo Magnetic Resonance Imaging (MRI) based studies were
devised to map hydration patterns and NP deformation in rotated positions of the
lumbar spine.
A pilot study (n=3), a normative rotation investigation (n=10) and normative lateral
flexion study (n=21) were conducted. All were undertaken with a substantially similar
methodology. Both T1 and T2 weighted lumbar MRI sequences were obtained in
sagittal plane positions with and without left trunk rotation. A pixel profile technique
was applied to the image data to determine direction and magnitude of NP deformation
at target intervertebral levels.
Data were derived using Image-J image analysis software (NIH, Bethesda, USA). Three
equidistant lines were placed across the mid disc region from which pixel data was
displayed, averaged in a Labview routine (National Instruments, Austin, USA) and
imported into Excel where direction and magnitude of NP deformation were compiled.
Intersegmental lateral flexion and rotation angles were measured and analysed for inter-
relationships with NP deformation.
To investigate the theme in non-normative populations, two cohort studies involving
subjects with age related IVD changes (n=11) and idiopathic scoliosis with secondary
lumbar curvature (n=12) were examined. Minor methodological refinements were made
to subject positioning and MRI slice angles to optimise segmental image and data
quality. The same image analysis method was applied to T1 and T2 weighted MRI
images to determine NP deformation patterns and directional predictability.
Page iii
Results
The cadaveric study reported greater ranges of axial rotation and joint separation in
lumbar segments in the presence of coronally oriented facets and degenerative disc
disease compared with sagitally oriented facets and discs without degenerative change.
The method used to gauge the deformation of the NP in different positions was
modified over the time course of the MRI studies and the following trends were
determined: (i) in normal young asymptomatic subjects positioned in the extremes of
flexion or extension within the MR imager, most NPs showed a tendency to deform
away from the area of greatest compression i.e. anteriorly in the case of lumbar
extension and to the convexity in the case of constrained lateral flexion, (ii) where
young subjects were positioned in left rotation plus either flexion or extension, there
was less certainty in predicting the deformation direction of the NP, (iii) there was
greater predictability of NP deformation direction relative to intersegmental lateral
flexion than axial rotation, (iv) in the case of older subjects with various stages of age
related disc disease, the trend was for similar NP deformation directional predictability
but reduced NP deformation magnitude and (v), in the case of the adolescents with
scoliosis all discs displayed a NP which deformed towards the concavity of the lateral
flexed apical disc segment.
Conclusions
The principal hypothesis that lumbar NP deformation direction was predictable relative
to positions in sagittal and coronal plane positions was accepted but was rejected for
axial plane positions. The magnitude of NP deformation was variable, being greater in
young subjects with well hydrated discs and less so in older IVDs with age related
changes and reduced hydration signal. The greatest NP deformation magnitude was seen
in the apical segments of secondary lumbar curves of subjects with the tri-dimensional
structural deformity of adolescent idiopathic scoliosis.
No relationships were evident between NP deformation magnitude and intersegmental
lateral flexion and rotation angles.
STATEMENT OF ORIGINALITY
Page iv
This thesis is presented in complete fulfilment for the degree of Doctor of Philosophy at
the University of Western Australia, through the Centre for Musculoskeletal Studies,
The School of Surgery.
The research project was developed by the author in consultation with supervisors
Winthrop Professor Kevin Singer, Director of the Centre for Musculoskeletal Studies,
The School of Surgery, the University of Western Australia; Dr Roger Price, Head of
Department, Medical Technology and Physics, Sir Charles Gairdner Hospital, and
Adjunct Professor, School of Surgery, The University of Western Australia; and Dr
Swithin Song FRACR, Head of Department, Magnetic Resonance Imaging and
Radiology, Royal Perth Hospital, Western Australia, who have also contributed to
editing of this thesis.
Planning and management of this study was the sole responsibility of the author.
Recruitment of volunteers was jointly undertaken by the author and Winthrop Professor
Kevin Singer in accordance with University informed consent and ethical standards.
The author conducted all aspects of testing with the exception of radiology. The author
independently analysed all data in consultation with supervisors.
The material comprising this thesis is the original work of the author towards the PhD
degree, unless otherwise stated. This thesis has not been submitted, either in part in
whole, for the award of any other degree at this or any other University.
Peter Fazey
July, 2011
ACKNOWLEDGEMENTS
Page v
Many People and organisations have contributed to the successful completion of this
thesis over an extended period. Thank you to all the individuals who volunteered to
participate in the numerous studies that comprise this thesis and those who, by way of
intelligent comment, opinion or passing remark, have unwittingly stimulated thoughts
that have shaped the direction of the thesis.
Paramount and heartfelt thanks must go to my primary supervisor Winthrop Professor
Kevin Singer for: his considerable patience and understanding of my extraneous
professional involvements; his continuous encouragement and reminding that the more
difficult and challenging times and tasks were indeed the most character forming; his
boundless patience in guiding and educating me along the research path – at times a
painfully slow and arduous journey for both; his facilitation of many aspects of all the
studies and the benefit of his extensive network, professional reputation and knowledge.
His vision alone was, thankfully, unwavering.
Thanks also to my secondary supervisor Adjunct Professor Roger Price whose rigorous
scientific and grammatical advice given with such good humour and gentle honesty
were both invaluable and greatly appreciated.
To co-supervisor Dr Swithin Song for his specific technical advice and facilitation of
access to the MRI unit at Royal Perth Hospital which was clearly fundamental to MRI
based research.
To Orthopaedic spinal surgeon Mr Peter Woodland for his continual, good natured
willingness to provide both clinical and editing advice as well as access to patient
records, his very professional and skilled staff, in particular orthotist Sandy Crameri,
and opening his spinal deformity clinic to me on many occasions.
To the brilliantly expert MRI technicians at Royal Perth Hospital, Barry Tanian and
Leonie Maddren for their considerable technical expertise and advice in developing the
MRI protocols given so freely and so early in the morning over weekends.
To Ray Smith for his technical and software advice and help, he always had the answer
and there was nothing he couldn’t fix.
Page vi
To my numerous co-authors in the various publications all contributed more than they
realise and made the whole greater than the sum of its parts. In particular Hiroshi
Takasaki, whose unstoppable drive was infectious and whose collaboration on several
publications invaluable. The thesis is greater as a result.
Finally, to Melissa whose support and continual encouragement motivated me when
nothing else could. This thesis is dedicated to her positivity and belief in me and is
testament to her strength and commitment.
THESIS PUBLICATIONS
Page vii
This thesis contains three published co-authored papers, five manuscripts and three co-
authored text chapters; their location within the text is indicated.
1. Peer reviewed journal papers and manuscripts
Fazey PJ, with: Song S, Mønsås Å, Johansson L, Haukalid T, Singer KP (2006). An
MRI investigation of intervertebral disc deformation in response to torsion.
Clinical Biomechanics 21, 538-542 (Appendix 4)
Fazey PJ, with: Takasaki H, Singer KP (2010). Nucleus pulposus deformation in
response to lumbar spine lateral flexion: an in vivo MRI investigation. European
Spine Journal 19(7): 1115-20
Fazey PJ, with: Takasaki H, May S, Hall T (2010). Nucleus pulposus deformation
following application of mechanical diagnosis and therapy: a single case report
with magnetic resonance imaging. Journal of Manual and Manipulative Therapy
18(3): 153-158 (Appendix 5)
Fazey PJ, with: Svansson GR, Day R, Price RI, Singer KP (2011). Pathoanatomical
influences on segmental rotation in the lumbar spine: Association between CT
imaging and 3D motion tracking. Submitted.
Fazey PJ, with: Song S, Price RI, Singer KP (2011). Internal derangement of the
lumbar intervertabral disc in response to torsion. Submitted.
Fazey PJ, with: Song S, Price RI, Singer KP (2011). Nucleus pulposus deformation
relative to rotation in middle aged lumbar intervertebral discs. Submitted.
Fazey PJ, with: Woodland P, Song S, Price RI, Singer KP (2011). The contribution of
lumbar nucleus deformation to the deformity of scoliosis: A preliminary
investigation. Submitted.
Fazey PJ, with: Woodland P, Song S, Price RI, Singer KP (2011). Herniated nucleus
pulposus – a quantitative 12 year longitudinal case study of paravertebral muscle
changes. Submitted.
2. Book chapters
Fazey PJ, with: Singer KP, (2004) Disc herniation - nonoperative management. In: HK
Herkowitiz, J Dvorak, G Bell, M Nordin, D Grob [eds] ISSLS Lumbar Spine. 3e.
Raven Lippincott, Philadelphia. pp 427-436 (Appendix 6)
Fazey PJ, with: Singer KP, Boyle J, (2005) Comparative anatomy of the zygapophysial
joints of the spine. In: J Boyling & G Jull [eds]. Greive's Modern Manual Therapy
3e. Churchill Livingstone. Edinburgh. pp 187-201 (Appendix 7)
Page viii
Fazey PJ, with: Khan K, Singer KP, (2011) Thoracic and Chest Pain. In: K Khan & P
Brukner [eds]. Clinical Sports Medicine, 4e. McGraw-Hill Education Australia
and New Zealand. In Press (Appendix 11)
3. Conference presentations
Fazey, PJ, Rotation effects on the lumbar intervertebral disc. Australian Physiotherapy
Association WA state conference: Perth 2003
Fazey, PJ, Effects of torsion on the lumbar intervertebral disc. Musculoskeletal
Physiotherapy Australia, National conference: Sydney 2003
Fazey, PJ, Intervertebral disc deformation in response to torsion. Spine Society of
Australia biennial scientific meeting: Auckland, New Zealand 2005
Fazey, PJ, Intervertebral disc deformation in response to torsion. Musculoskeletal
Physiotherapy Australia Biennial National conference: Brisbane 2005 (Appendix
8)
Fazey, PJ, Does sustained lumbar rotation induce nucleus pulposus deformation in a
predicable manner ? – an MRI investigation. World Confederation for Physical
Therapy International Congress, Vancouver, Canada 2007.
Fazey, PJ, Nucleus Pulposus deformation in response to rotation – an in vivo MRI
investigation. 6th
International Meeting of Physical Therapy Science, Perth 2008.
Fazey, PJ, with: Song S, Price RI, Singer KP. Lumbar intervertebral disc deformation
in response to rotation: an age contrast study employing MRI. American Physical
Therapy Association National Conference, Baltimore 2009 (Appendix 9)
Fazey, PJ, with: Breidahl WH, Singer KP,Fatal fracture disclocations associated with
an ankylosed spine: A case report. Spine Society of Australia scientific meeting.
Adelaide, Australia 2009 (Appendix 10)
DECLARATION FOR THESIS CONTAINING PUBLISHED WORK
This thesis contains published co-authored work comprising chapters 4, 6 and 9 and
appendices 4 – 7. These papers and chapters were published during the course of
enrolment for this thesis investigation in collaboration with supervisors who provided
editorial advice and input in their submission for publication. As such the work
contained within these chapters was by greater majority the work of the author at
submission for publication.
Peter Fazey Professor Kevin Singer
PhD candidate Coordinating supervisor
TABLE OF CONTENTS
Page ix
ABSTRACT.......................................................................................................................i
STATEMENT OF ORIGINALITY.................................................................................iv
ACKNOWLEDGMENTS.................................................................................................v
THESIS PUBLICATIONS..............................................................................................vii
TABLE OF CONTENTS.................................................................................................ix
LIST OF APPENDICES..................................................................................................xi
GLOSSARY OF ABBREVIATIONS.............................................................................xii
GLOSSARY OF DEFINITIONS...................................................................................xiii
CHAPTER 1
Introduction.....................................................................................................................I-1
CHAPTER 2
Review of Literature......................................................................................................II-1
CHAPTER 3
Methods........................................................................................................................III-1
CHAPTER 4
Pathoanatomical influences on segmental rotation in the lumbar spine: Association
between CT imaging and 3D motion tracking ............................................................IV-1
CHAPTER 5
Internal derangement of the lumbar intervertabral disc in response to torsion.............V-1
CHAPTER 6
Nucleus pulposus deformation in response to lumbar spine lateral flexion: an in vivo
MRI investigation........................................................................................................VI-1
CHAPTER 7
Nucleus pulposus deformation relative to rotation in middle aged lumbar intervertebral
discs............................................................................................................................VII-1
CHAPTER 8
The contribution of lumbar nucleus deformation to the deformity of scoliosis: A
preliminary investigation............................................................................................VII-1
CHAPTER 9
Herniated nucleus pulposus – a quantitative 12 year longitudinal case study of
paravertebral muscle changes....................................................................................VIII-1
Page x
CHAPTER 10
Discussion.....................................................................................................................X-1
CHAPTER 11
Conclusions and recommendations..............................................................................XI-1
APPENDICES
LIST OF APPENDICES
Page xi
APPENDIX 1 Human Research and Ethics Committee application form
APPENDIX 2 Participant information and consent
APPENDIX 3 MRI consent form
APPENDIX 4 Fazey PJ, with: Song S, Mønsås Å, Johansson L, Haukalid T, Singer
KP (2006). An MRI investigation of intervertebral disc deformation in
response to torsion. Clinical Biomechanics 21, 538-542
APPENDIX 5 Fazey PJ, with: Takasaki H, May S, Hall T (2010). Nucleus pulposus
deformation following application of mechanical diagnosis and
therapy: a single case report with magnetic resonance imaging.
Journal of Manual and Manipulative Therapy 18(3): 153-158
APPENDIX 6 Fazey PJ, with: Singer KP, (2004) Disc herniation - nonoperative
management. In: HK Herkowitiz, J Dvorak, G Bell, M Nordin, D
Grob [eds] ISSLS Lumbar Spine. 3e. Raven Lippincott, Philadelphia.
pp 427-436
APPENDIX 7 Fazey PJ, with: Singer KP, Boyle J, (2005) Comparative anatomy of
the zygapophysial joints of the spine. In: J Boyling & G Jull [eds].
Greive's Modern Manual Therapy 3e. Churchill Livingstone.
Edinburgh. pp 187-201
APPENDIX 8 Fazey, PJ, Intervertebral disc deformation in response to torsion.
Musculoskeletal Physiotherapy Australia Biennial National
conference: Brisbane 2005
APPENDIX 9 Fazey, PJ, with: Song S, Price RI, Singer KP. Lumbar intervertebral
disc deformation in response to rotation: an age contrast study
employing MRI. American Physical Therapy Association National
Conference, Baltimore 2009
APPENDIX 10 Fazey, PJ, with: Breidahl WH, Singer KP,Fatal fracture disclocations
associated with an ankylosed spine: A case report. Spine Society of
Australia scientific meeting. Adelaide, Australia 2009
APPENDIX 11 Fazey PJ, with: Khan K, Singer KP, (2011) Thoracic and Chest Pain.
In: K Khan & P Brukner [eds]. Clinical Sports Medicine, 4e.
McGraw-Hill Education Australia and New Zealand. In Press.
GLOSSARY OF ABBREVIATIONS
Page xii
A-P Antero-posterior
AF Anulus Fibrosus
CSA Cross Sectional Area
CT Computerised Tomography
CV Coefficient of Variation
FSU Functional Spinal Unit
HNP Herniated Nucleus Pulposis
IVD Intervertebral Disc
IVF Intervertebral Foramen
LBP Low Back Pain
LF Lateral Flexion
MRI Magnetic Resonance Imaging
mm Millimetre
MPa Megapascal
NP Nucleus Pulposus
P-A Postero-anterior
ROI Region of Interest
SF Side Flexion
US Ultrasonography
VB Vertebral Body
ZJ Zygapophysial Joint
Note: Anatomical spelling in this thesis is consistent with that listed in:
Terminologia Anatomica: International Anatomical Terminology, New York: Thieme
Medical Publishers, 1998.
The terms lateral flexion and side flexion are used interchangeably in this thesis.
GLOSSARY OF DEFINITIONS
Page xiii
Arthrokinematics: Refers to articular mechanics (Williams et al., 1989). It typically
describes the direction and characteristics of movement or component parts of
movements of joints.
Axial rotation: Refers to the movement of a vertebral segment around the ‘y’ axis. The
direction is taken as that of a vertebral segment relative to its subjacent neighbour
(White & Panjabi, 1990).
Coupled (conjunct) movement: Occurs when rotation or translation about or along one
axis is consistently associated with rotation or translation about or along a second axis
(White & Panjabi, 1990). It is described in terms of direction.
Creep: Time dependent tissue deformation while under constant load. It usually occurs
as water is gradually expelled from the loaded tissue (White & Panjabi, 1990).
Deformation: Refers to a change in form or shape of a body. In the context of this
thesis with reference to the nucleus pulposus (NP) it refers to a change in NP shape
resulting from load application.
Directional predictability: In the context of this thesis this concept refers to how
predictably the nucleus pulposus will deform in a given direction within the confines of
the anulus.
Extension: Refers to regional spinal motion or segmental rotation or position in a
posterior direction from a given starting point. It includes both posterior segmental
rotation and posterior translation.
Flexion: Refers to regional spinal motion or segmental rotation or position in an
anterior direction from a given starting point. It includes both anterior segmental
rotation and anterior translation.
Page xiv
Hydration pattern: Refers to the variable distribution of hydration throughout a
prescribed region. In the context of this thesis that region is the intervertebral disc.
Lateral Flexion: Refers to regional spinal motion or segmental rotation or position in
the coronal plane from a given starting point. The terms lateral flexion and side flexion
are used synonymously.
Migration: Refers to the movement or displacement of material from one location to
another.
Osteokinematics: The study of bone movement (Williams et al., 1989). It is described
relative to standard axes or adjacent structures.
Spinal segmental Instability: The loss of the ability of the spine under physiologic
loads to maintain its pattern of displacement so that there is no initial or additional
neurological deficit, no major deformity, and no incapacitating pain (White and Panjabi,
1990, p278).
Common biomechanical terms are used throughout the thesis with reference to the
standard text, White and Panjabi, 1990.
White A, Panjabi M. Clinical Biomechanics of the Spine, 2 ed. Philadelphia: Lippincott,
1990.
Williams PL, Warwick R, Dyson M, Bannister LH. Gray's Anatomy, Edinburgh:
Churchill Livingstone, 1989.
CHAPTER 1
Page I-1
Introduction
Low back pain (LBP) is highly prevalent in the community with an 85% lifetime and
35% point prevalence (Nachemson, 1999). Back pain is frequently attributed to
disorders of the intervertebral disc (IVD) (Gunzburg et al., 1991; van Tulder et al.,
2000) including degenerative change and internal disruptions of the disc resulting in
herniation. These may occur subsequent to acute injury or gradually due to repeated
minor trauma or age (Bogduk & Twomey, 1987). One mechanism of injury that is
commonly proposed involves rotary or twisting motions, often in combination with
loading of the spine (Farfan et al., 1972).
Intersegmental lumbar rotation is primarily limited by the orientation of the articular
facets and the collagenous fibre orientation of the anulus. The central region or nucleus,
is normally well-hydrated and behaves as a hydrostatic mechanism (Buckwalter, 1995).
Compression causes the nucleus pulposus (NP) to alter from a spherical shape to an
ovoid conformation (Adams et al., 1996). This exerts a circumferential pressure on the
walls of the surrounding collagen rings of the anulus fibrosus (AF), evenly distributing
the load across the disc and vertically to adjacent vertebral bodies via the end-plates. It
is also apparent that the NP, in response to asymmetric loading, will migrate toward the
area of least load (Krag et al., 1987; Kramer, 1981). Discs can undergo age-related
degeneration, with associated reduction in the degree of hydration (Modic & Ross,
2007). This jeopardises the effectiveness of load distribution, often causing abnormal
localised concentration of disc pressure which may result in ruptured or herniated discs,
or disruption of the vertebral end-plates. Consequently, IVD investigations employing
detailed imaging modalities and assessment of hydration will assist in ascertaining the
status of disc condition as it affects internal mechanics.
Many studies have been published on sagittal movement, and somewhat less on lateral
flexion; there is, however, a paucity of literature on the effects of rotation on internal
IVD mechanics and no reports of the effects of rotation on nucleus position or
deformation .
Chapter 1 – Introduction
Page I-2
Reports in the literature of migration of NP material within the confines of the AF
boundaries may not capture internal fluid redistribution within the NP and resultant NP
deformation. This subtle but important difference is elaborate in Chapter 10, section
10.2.1, pX-2.
The IVD exhibits time and rate-dependent and viscoelastic biomaterial properties. It is
assumed that mechanical loads in different positions influence the morphology and
internal structure of the IVD (White & Panjabi, 1990). Back exercises and passive
movement techniques have been prescribed on the basis of this concept (Cyriax &
Cyriax, 1993; McKenzie, 1981). McKenzie (1981) recommends the use of lumbar
extension exercises on the basis that the NP is purported to migrate anteriorly, thereby
distancing the NP from pain sensitive structures in an injured posterior anulus fibrosus.
Moreover, flexion exercises are believed to enlarge the cross sectional area of the neural
canal and intervertebral foramina, thereby decreasing mechanical stimulus of pain
sensitive structures contained within (White & Panjabi, 1990).
The trend towards an anterior NP migration following sagittal movements has also been
supported in several in vivo Magnetic Resonance Imaging (MRI) studies (Brault et al.,
1997; Edmondston et al., 2000; Fennell et al., 1996). However, the trend has not always
been consistent and segmental variations are reported (Edmondston et al., 2000; Fennell
et al., 1996). These studies have also used a variety of techniques to isolate and define
the NP or its boundaries, ranging from visual inspection to profiling the MRI pixel
intensity. This latter method, while effectively measuring hydration levels and
distribution, is limited to a single image sample of the IVD in one plane only and may
not represent accurately the total hydration distribution within the entire IVD.
Migration of the NP within the IVD in response to load distribution during axial
rotation remains unknown. However, rotation is assumed to change the foraminal
dimension by decreasing width and area on the ipsilateral side and increasing the
foraminal space on the contralateral side (Fujiwara et al., 2001). Nevertheless, the
mechanism of rotation is more complex as the concept of coupled movement must be
considered. Axial rotation is always combined with some degree of lateral flexion
(Pearcy et al., 1984). In the normal spine, rotation and lateral flexion are usually
coupled to the same side in flexion, whereas this coupling occurs to opposite sides in
Chapter 1 – Introduction
Page I-3
neutral and spinal extension (Pearcy & Tibrewal, 1984). Some authors claim coupled
motion at the lumbosacral junction occurs in the opposite manner and that at L4-5
coupling may vary unpredictably between individuals (Vicenzino & Twomey, 1993).
The direction of lateral flexion coupling may influence compression distribution within
the IVD, and consequently direction of NP migration during rotation. It is also reported
that segmental morphology influences axial rotation range according to different
positions within the range of available sagittal postures (Pearcy & Hindle, 1991).
This thesis aims to examine the effect of rotation on the intervertebral disc with
reference to the relationship between axial and coronal rotation via a series of unique in
vivo studies of intradiscal hydration patterns.
Improved understanding of the effects of rotation in vivo will contribute original
insights to the body of knowledge relevant to both aetiology and management of the
debilitating and costly condition that is low back pain.
In this study it is hypothesised that:
1. The nucleus pulposus will deform with rotation in a predictable fashion as a
function of coupled motion in normal individuals;
2. This model can be elaborated in physiological lateral flexion positions, and in
established scoliosis;
3. The reliability of predicting NP deformation in older individuals will be less
certain, dependent on the degree of established disc degeneration.
The primary study series was designed to generate hypotheses and raise questions
leading to subsequent more detailed investigations.
Part 1 of this thesis begins with a description of the methods employed through the
studies contained within (chapter 3). This includes explanation of the subtle
refinements to the methods made through the course of conducting the studies, as
development of the concept and testing of the hypotheses highlighted additional
variables and improved ways to examine the questions. The individual studies begin
with chapter 4 which describes the hypothesis generating study; a computerised
tomography (CT) ex vivo cadaveric evaluation of the biomechanics of axial rotation
Chapter 1 – Introduction
Page I-4
which considers pathoanatomical influences of degeneration relative to the IVD and
articular facet orientation. This is followed by an introduction to a novel method of
examining in vivo intradiscal hydration patterns utilising pixel intensity profiles derived
from Magnetic Resonance Imaging (MRI) and employs this to assess the intradiscal
effect of positional change relative to segmental rotation within sagittal, coronal and
axial planes in a cohort of young asymptomatic subjects (chapter 5). Chapter 6
examines in more detail the effect of a primary positioning in the coronal plane on NP
deformation, indexed by hydration pattern changes in the NP.
Part 2 integrates this understanding of biomechanics and intradiscal change into the
context of spinal pathology. Chapter 7 introduces the variable of age-related
degenerative change and its influence on predictability of rotation induced NP
deformation direction and magnitude. Chapter 8 evaluates NP deformation in
secondary lumbar curves of subjects with idiopathic scoliosis which includes deformity
in both the coronal and axial planes. Chapter 9 focuses on a single case study
subsequent to a lumbar rotation induced IVD trauma, with sequential imaging and
analysis over an extended period of recovery.
Chapter 10 discusses the results in context and draws common themes and trends
together while also acknowledging limitations in both method and results which qualify
the conclusions that may be drawn. Chapter 11 summarises and draws conclusions
which help inform the recommendations for future related studies and further questions
raised.
Following this introduction chapter 2 provides an overview of the background
literature relevant to parts 1 and 2 of this thesis.
Chapter 1 – Introduction
Page I-5
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Livingstone, 1987.
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McKenzie RA. The Lumbar Spine. Mechanical Diagnosis and Therapy. Wellington:
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Modic MT, Ross JS. Lumbar degenerative disk disease. Radiology 2007; 245(1): 43-61.
Nachemson A. Back Pain: Delimiting the problem in the next millenium. International
Journal of Law and Psychiatry 1999; 22: 473-90.
Pearcy M, Hindle R. Axial rotation of lumbar intervertebral joints in forward flexion.
Proc Inst Mech Eng [H] 1991; 205(4): 205-9.
Pearcy M, Portek I, Shepherd J. Three-dimensional x-ray analysis of normal movement
in the lumbar spine. Spine 1984; 9(3): 294-7.
Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine
measured by three-dimensional radiography. Spine 1984; 9: 582-87.
van Tulder M, Malmivaara A, Esmail R, Koes B. Exercise Therapy for Low Back Pain:
A Systematic Review Within the Framework of the Cochrane Collaboration
Back Review Group. Spine 2000; 25(21): 2784-96.
Vicenzino G, Twomey L. Sideflexion and induced lumbar spine conjunct rotation and
its influencing factors. Australian Journal of Physiotherapy 1993; 39: 299-306.
Chapter 1 – Introduction
Page I-6
White A, Panjabi M. Clinical Biomechanics of the Spine, 2 ed. Philadelphia: Lippincott,
1990.
CHAPTER 2
Page II-1
Review of Literature
2.1 Overview
This literature review is divided into three sections. Section 1 will introduce the
relevant anatomy and physiology of the lumbar vertebral column as it relates to motion.
It includes a review of biomechanics of the lumbar region, with a focus on rotation, the
concept of complex coupled motion and IVD mechanics. Section 2 examines the
literature relevant to age related changes and degeneration of the spine and how that
impacts upon the biomechanics elaborated in Section 1. Section 2 also discusses other
pathologies in which mechanics are altered such as scoliosis and herniated nucleus
pulposus. Section 3 discusses imaging relative to investigations reported through the
body of the thesis in addition to the measurement techniques that have been employed
to analyse medical images. A summary of the review follows which highlights those
key questions arising from the literature which are subsequently investigated through
the thesis.
The literature reviewed in this chapter is confined largely to that which relates directly
to the subsequent thesis investigations.
2.1 Section 1: Anatomy, Physiology and Biomechanics
2.1.1 Anatomy
As form and function are intimately related, the purpose of this section is to review
basic spinal anatomy, knowledge of which is fundamental to an understanding of
function and mobility, including rotation. It is not intended to provide a comprehensive
review of spinal anatomy, rather it is restricted to those anatomical aspects relevant to
the study presented in this thesis. For a more thorough review of lumbar spine anatomy
the reader is directed to standard texts (Bogduk, 2005; Bogduk & Twomey, 1991).
The human spine is designed to provide stability while maintaining functional mobility
of both the axial and appendicular skeletons. In doing so it must also efficiently transmit
force and momentum during motion, especially ambulation. It has developed particular
anatomical dimensions and characteristics specific to mammals that equip it for bipedal
Chapter 2: Review of Literature
Page II-2
activity (Boszczyk et al., 2001). The spine is divided into three regions cervical,
thoracic and lumbar which integrate functionally despite markedly different roles.
The lumbar spine comprises five vertebrae and their intervening discs, each contributing
to the roles of rigidity and mobility. The functional unit of the lumbar spine (Figure 2.1)
comprises two adjacent vertebrae, the intervening intervertebral disc and endplates, the
paired zygapophysial joints, all adjoining ligaments, adjacent muscles and includes the
contents of the spinal canal, intervertebral foramen and areas between transverse and
spinous processes, (Schmorl & Junghanns, 1959).
Figure 2.1: An axial cryosection through L3-4 depicting the paired zygapophysial
joints, the adjacent intervertebral disc, and associated pre- and post-ventral musculature.
The anular layers of the disc are shown along with remnant neural elements of the cauda
equina within the dura. [AF = anulus fibrosus; P = psoas; M = multifidus; D = dura; Z =
zygapophysial joint]. (Image used with permission from: Dr G.Groen, University of
Utrecht, The Netherlands).
AF P
M
Z
D
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2.1.1.2 The bony vertebra
To meet its cardinal role of rigidity, the lumbar vertebra comprises the vertebral body
(VB) anteriorly and the neural arch posteriorly.
To resist compression the VB consists of a cortical shell to constrain marrow and
cancellous bone and is essentially rectangular and semi lunar in lateral and transverse
sections respectively. The concave outer shell of cortical bone is strengthened by an
internal architecture of struts (trabeculae) running both vertically and horizontally. The
outer rim of the superior and inferior surfaces is of smoother bone called the ring
apophysis – a secondary ossification centre of the vertebral body (Schmorl &
Junghanns, 1959). The posterior column, connected to the anterior via the pedicles,
comprises the laminae, spinous process, transverse processes and articular facets, or
zygapophysial joints. The motion control function of the articular facets will be
discussed separately in section 2.1.2.2.
2.1.1.3 The intervertebral disc
The intervertebral disc is situated in the interbody space. It consists of the anulus
fibrosus, the nucleus pulposus and the vertebral end plates. The latter bound the disc
superiorly and inferiorly with predominantly hyaline cartilage approximately 1mm
thick. With a horizontal lamellar arrangement the end plates serve to contain the fluid
nucleus and provide a pathway for nutrient transfer between the spongiosa and the
central disc via small vascular buds (Giles & Singer, 1997).
The anulus contains 10 – 20 concentric rings of circumferential collagenous lamellae.
Type 1 collagen predominates in the periphery and Type 2 centrally. The peripheral
fibres connect the ring apophyses above and below while the central fibres act as a
meshwork capsule to contain the nucleus (Schollum et al., 2008). The lamellar fibres are
angled obliquely at approximately 65° to the sagittal plane. Each adjacent lamella is
oriented in the opposite direction to its neighbour. The oblique orientation places the
fibres optimally to resist torsion and translation (Bullough, 2007) (Figure 2.2). The
degree to which the anulus does so is arguable with respect to torsion especially in
flexion, the combination of which is reported to afford greater resistance to radial tears
(Veres et al., 2010a, b). Recently described radial connections between lamellae have
been suggested to play a role in nucleus pulposus biomechanics (Schollum et al., 2009).
Chapter 2: Review of Literature
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The nerve supply to the intervertebral disc is meager and predominantly concentrated in
the periarticular connective tissue and central endplate (Fagan et al., 2003).
Figure 2.2: Anulus lamellae are oriented to resist translation and torsion (From
Bullough 2007)
2.1.1.4 The nucleus pulposus
The nucleus pulposus’ primary function is load attenuation. The NP consists of (in order
of magnitude) water, proteoglycans and a loose collagen matrix. Its fluid properties
disperse axial load to the periphery to brace the inner anular fibres. The nucleus behaves
as a hydrostatic mechanism deforming towards the area of least compression (Keyes &
Compere, 1932; McKenzie & May, 2003). How it deforms in response to torsion in
vivo is unclear. Normal IVD height (approximately 10mm) is largely maintained as a
function of the fluid filled nucleus and varies with diurnal loading (Malko et al., 1999).
Fluid loss with compressive loading occurs primarily in the posterior anulus (30%) and
the NP (15%) (McMillan et al., 1996). Proportional content and function of the
ultrastructure of the IVD as described by Lundon and Bolton are summarized in Table
2.1 (Lundon & Bolton, 2001).
2.1.1.5 The articular facets
The articular facets of adjacent vertebrae interlock to form the synovial zygapophysial
joints. These primarily control and limit motion into rotation and anterior translation
and also accept a minority weightbearing role in erect standing (Adams & Hutton, 1980;
Shirazi-Adl, 1991). Loading is increased with increasing extension moment between the
tip of the inferior articular process and the pars interarticulares of the subjacent level
(Yang & King, 1984). The articular surfaces are oriented more sagitally in the cranial
lumbar segments and progressively coronally in the more caudal. A concomitant medial
orientation ensures joint surface compression resists anterior translation during flexion.
Partial disengagement occurs in flexion exposing the inferior articular surface which
remains protected by a synovial fold.
Chapter 2: Review of Literature
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Segmental axial rotation results in compression of the contralateral inferior facet against
the contralateral superior facet of the subjacent level. Simultaneously the ipsilateral joint
space widens thereby tensioning the joint capsule.
Sagittal facetal orientation constrains axial rotation to a greater extent than coronal
orientation (Haughton et al., 2002; Krismer et al., 1996; Singer et al., 2001).
Facet asymmetry is common. The definition of excessive asymmetry, or ‘tropism’, is
arbitrary but has been attempted mathematically (Boden et al., 1996). Tropism has been
investigated for its relationship with disc herniation (Karacan et al., 2004; Ko & Park,
1997; Lee et al., 2006; Park et al., 2001) and degenerative change (Boden et al., 1996;
Grogan et al., 1997; Murtagh et al., 1991; Newton et al., 1993; Noren et al., 1991;
Vanharanta et al., 1993).
Findings vary as to whether tropism predisposes to degenerative change however it has
been correlated with disc pathology including prolapse (Farfan & Sullivan, 1967). This
is likely difficult to assess due to the common and multifactorial nature of degenerative
change in the lumbar spine.
Lumbar facets develop symmetrically in children with a variation in joint maturity age
between genders. Females cease development at age 12 while males continue to develop
beyond this age. This differs from the thoracic spine where asymmetry is common in
children and attributed to the influence of upper limb activities (Masharawi et al.,
2008a; Masharawi et al., 2008b). This influence is dramatically less in the lumbar spine
putatively due to its relative distance from the upper limbs. Consequently development
of facet asymmetry is suggested to be a post adolescence occurrence (Masharawi et al.,
2009). Reichmann, however, reported that some adult joint features are present at birth
implying a prenatal genesis for the process of development (Reichmann, 1971b).
Tropism should not influence the ability of the facets to constrain segmental rotation.
However the more sagittally oriented facet would take the greater compressive force
under torsion strain and fail before an adjacent coronally oriented facet in ex vivo
failure load experimentation (Adams et al., 2002).
2.1.1.6 Muscles of the lumbar region
The muscles of the spine can be divided regionally into deep, intermediate and
superficial. It is the intermediate and deep layers that relate specifically to the lumbar
Chapter 2: Review of Literature
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spine. The intermediate layer consists primarily of the erector spinae group. This
comprises iliocostalis, longissimus and spinalis. The erector spinae group arises from
the iliac crests, the posterior sacrum, the sacral and inferior lumbar spinous processes
and the supraspinous ligament. Their primary action is to extend the spine but acting
unilaterally may laterally flex the spine. These muscles may also contribute via motion
coupling (refer section 2.1.2.3) to rotation, though the direction would be variable
(Moore, 1997).
The deep layer comprises multifidus and rotatores. Multifidus has both unisegmental
and polysegmental fascicles arising from the mammillary process of one vertebra and
extending to the spinous process of an adjacent vertebra or one up to several segments
distant. It is an extensor of the spine but may unilaterally contribute to rotation towards
that side. Multifidus has also been ascribed a segmental stabilizing role (MacDonald et
al., 2009; Richardson et al., 2002). Rotatores arises from transverse processes and
extends to the junction of the lamina and transverse process of the level above. It will
also assist rotation ipsilaterally (Lee et al., 2005).
There also exists a minor deep layer of small intersegmental muscles; interspinales and
intertransversarii. The former attaches to adjacent spinous processes and the latter to
adjacent transverse processes. Interspinales has been implicated in extension and
rotation while intertransversarii is a lateral flexor and therefore, by default through
coupled motion, also a rotator (Bogduk & Twomey, 1987).
Other than the muscles described that have attachment directly to the spine there are
other rotators of the trunk that can generate considerable torque and as such induce
segmental rotation in vivo. These include the oblique abdominals and latissimus dorsi.
Little literature reports the segmental effect of large torque producing muscles though it
is reported in elite sports (Burnett et al., 2008; Burnett et al., 1998).
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TABLE 2.1. Ultrastructure of the normal intervertebral disc.
Structure/component
Water Proteoglycans (PGs) Collagen Elastin Cells
Nucleus Pulposus
(NP)
70-90% 65% dry weight of NP
PGs are key to the inherent
mechanical prop
erties of the NP
PGs present in the NP
include hyaluronic acid,
chondroitin sulfate, and
keratan sulfate
15-20% dry weight
Exists as an irregular
network that binds PGs
Types II (85%) and small
amounts of types III,V,I
and XI collagens are found
in the NP
Small quantities of fibres with
no specific orientation
Chondrocytes (responsible
for production of matrix
including PGs and collagen
components)
Concentration of chondrocytes
in the NP is less than that of
the surrounding AF, and they
are found mainly in the
vertebral end plate area
Anulus Fibrosus
(AF)
60-70% 15-20% of dry weight of
AF
PG gel, together with cells
and elastin, occupies
the spaces between
the collagen fibers of the
lamellae of the AF; this
acts to bind the lamellae
together and contributes
to the stiffness of the AF
50-60% dry weight of AF
Type I (predominant
collagen of AF providing
resistance to tension) and
types II,III,V,VI and IX are
found in the AF
Concentration of type II
collagen progressively
increases towards the
centre of the anulus as type
I collagen concentration
decreases
10% of dry weight of the AF
Fibres are arranged in a
circular, oblique and vertical
manner within the lamellae
Elastin fibres are closely
related to the densely packed
collagen fibres; they are
oriented parallel to those fibres
Elastin confers
resilience/elasticity to AF
Chondrocytes and fibroblasts
are dispersed among the
collagen fibres of the
individual lamellae and
between the lamellae
themselves
Fibroblasts are found
predominantly in the
periphery of the AF;
chondrocytes towards the NP
Adapted from Lundon and Bolton, 2001
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2.1.1.7 Axial rotation
The design features of the spine appear to be biased towards limitation and control of
axial rotation. While this may be necessary to avoid the deleterious effects of excessive
rotation it is also of benefit in trunk motion and translation of energy. Farfan has
postulated that by limiting rotation the spine is able to more effectively transmit force
generated by arm and shoulder swinging to the pelvis and lower limbs, thereby
powering ambulation (Farfan, 1973, 1995). Intersegmental torsion in the flexed position
is reported to increase nucleus pressure and the anulus’ resistance to radial tears by
approximately 50% (Veres et al., 2010a).
The extent to which the various anatomical structures limit rotation has been argued in
the literature. While it is claimed that the facets are the primary restraint to rotation
(Adams & Hutton, 1981a) the nucleus is also reported as providing the greatest
percentage of rotary stability (White & Panjabi, 1990). Earlier work (Farfan et al., 1970)
has suggested that microfailure of anular fibres at 3° of intersegmental rotation indicates
the major role of the anulus in rotation limitation. Later Adams and Hutton (1983b),
disputed this assertion, claiming that the primary anatomical restraint is in fact the
articular facets, since anular failure does not occur until 9° of rotation (Adams &
Hutton, 1983b).
Gunzburg et al (1992) have reported the role of capsuloligamentous structures in axial
rotation following sequential ex vivo lesioning and conclude that zygapophysial joint
capsules contribute to axial rotation constraint in flexion but that the posterior anulus
and posterior longitudinal ligaments are the primary restraint in flexion (Gunzburg et
al., 1992).
The posterior anulus is also reportedly afforded protection in rotation by the sagittal
configuration of the facet surfaces and in flexion by the capsular ligaments (Adams &
Hutton, 1983b).
The anatomy of the lumbar spine and the inextricable link between form and function
indicate a need to permit controlled rotation. Clearly there must exist a balance from
which optimal mechanical benefit and sufficient control to avoid injury will be derived.
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2.1.2 Biomechanics
This section addresses only the literature relevant to the biomechanical principles
referred to in this thesis, in particular that which relates to axial rotation. For a more
detailed description of spinal biomechanics the reader is directed to the definitive texts
(Adams et al., 2006; White & Panjabi, 1990).
2.1.2.1 Osteokinematics
The bony vertebra rotates around x,y and z axes. This is accompanied by translatory
motion along a horizontal plane (Figure 2.3). Normal ranges of rotation in each plane
have been measured with stereographic radiography (Dvorak et al., 1991; Miles &
Sullivan, 1961; Pearcy et al., 1984; Pearcy & Tibrewal, 1984; Reichmann, 1971a) and
MRI with or without fluoroscopy (Haughton et al., 2002; Li et al., 2009; Xia et al.,
2009) segmentally (Yamamoto et al., 1989) as well as regionally (Russell et al., 1993).
In vivo and ex vivo segmental ranges are comparable in the published literature.
Axial rotation occurs about an axis through the posterior one third of the IVD. The
segmental range is dependent upon facet orientation; increasing with greater coronal
bias (Haughton et al., 2002; Singer et al., 2001; Singer et al., 1989; Singer et al., 1996).
Figure 2.3: Axes and directions of rotation and translation of lumbar vertebra (Adapted
from Bogduk & Twomey, 1987).
Chapter 2: Review of Literature
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Ex vivo studies of unilateral rotation to failure demonstrate a migration of the rotational
axis towards the contralateral facet when torsion load is taken beyond physiological
limits (Adams & Hutton, 1981a; Wachowski et al., 2009). Failure typically occurs at the
compressed facet in the first instance (Farfan et al., 1970).
Ranges of axial rotation vary with sagittal plane positioning. Mid range flexion is
associated with marginally increased ranges (Pearcy et al., 1984; Pearcy & Tibrewal,
1984; Pearcy, 1993) while end range extension or full flexion is associated with reduced
ranges (Burnett et al., 2008; Pearcy & Hindle, 1991b). Likely this is due to the locking
of articular facets at the end range of extension, the relative unlocking in mid range
flexion and the re-locking at end range flexion where translation forces the medially
inclined facets against their subjacent partner.
It has, however, also been demonstrated that maximal decreased axial twist stiffness and
increased axial twist angle occur in maximal flexion (Drake & Callaghan, 2008). This
finding does not support the claim for greater motion in mid range flexion but may
reflect a discrepancy between segmental ex vivo and regional in vivo studies.
Pressurisation of the nucleus in an ex vivo study of isolated ovine disc constructs was
associated with tears of the outer anulus at the end plate junction in flexed specimens
and between the inner anulus and end plate in neutrally positioned segments (Veres et
al., 2010b). The relevance of this injury pattern to human in vivo conditions is unclear.
Translation typically occurs in the direction of segmental rotation about the x and z
axes. In primary axial rotation about the y axis, translation may occur in the direction of
coupled z axis rotation (refer Figure 2.3).
2.1.2.2 Arthrokinematics
A functional spinal unit (FSU) comprises two vertebra and the intervening intervertebral
disc and surrounding ligaments and muscles (refer section 2.1.1). The articular
components are considered to be the paired synovial posterior zygapophysial joints and
the interbody joint. The latter will be considered in more detail elsewhere in this thesis
in consideration of the intervertebral disc mechanics.
Chapter 2: Review of Literature
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Anterior vertebral rotation causes the inferior articular facets to ride cranially on the
superior articular facets of the vertebra below (Stokes, 1988). This shear movement is
limited by compression of the anterior anulus and stretch of the zygapophysial joint
capsule. The capacious nature of the capsule superiorly and inferiorly allows
considerable movement (Singer et al., 2004). The articular surfaces are left somewhat
exposed but are protected by meniscoid inclusions; a fold of synovium that resides in
the polar recesses of the articular surfaces.
Posterior rotation results in caudal glide of the inferior articular facets on their
neighbour. This is limited by contact between the tip of the inferior articular process and
the lamina of the vertebra below (Adams & Hutton, 1980).
Axial rotation widens the intervertebral foramen (IVF) (Fujiwara et al., 2001) and
zygapophysial joint space on the ipsilateral side and compresses on the contralateral.
The thicker posterior portion of the lumbar zygapophysial joint capsule helps resist
excessive torsion (Singer et al., 2004) (Appendix 7).
Articular asymmetry of the zygapophysial joints, or ‘tropism’, occurs at the cervico-
thoracic junction (Boyle et al., 1996) and most commonly at the lumbo-sacral and
thoraco-lumbar junctions (Singer et al., 2004). Tropism may predispose the segment to
rotation towards the coronally oriented side during torsion coupled with posteroanterior
shear force.
For a detailed examination of zygapophysial joint anatomy the reader is directed to
Appendix 7.
2.1.2.3 Coupled motion
Coupled motion occurs when primary motion in one plane induces motion in another
(Lovett, 1905). It is a well documented and accepted mechanical property of the spine
(Cholewicki et al., 1996; White & Panjabi, 1990). The key literature on lumbar spine
coupling considers the relationship between lateral flexion and axial rotation; for every
degree of axial rotation there occurs approximately two degrees of lateral flexion
(Panjabi, 1989).
Controversy exists as to the direction of coupling in the lumbar spine (Cholewicki et al.,
1996). Some report a predominant contralateral pattern (Russell et al., 1993; Steffen et
Chapter 2: Review of Literature
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al., 1997) while Vicenzino and Twomey (1993) claim a mixed pattern with segmental
variation.
Most studies investigating coupled motion are ex vivo and postulate that geometry
accounts for coupling directional preference (Scholten & Veldhuizen, 1985). Clearly
this does not consider the influence of contractile element action. In vivo evidence
exists to claim a predominant ipsilateral pattern which varies between maximal and sub
maximal voluntary contraction of trunk rotators (Ng et al., 2001). The lumbar extensor
muscles reportedly contribute only 5% of axial torque in the trunk; the majority being
attributed to the oblique abdominal group (Macintosh et al., 1993).
Finite element modeling has been used by Little et al (2008) to compare in vivo with ex
vivo three dimensional motion coupling. This study has confirmed consistency for all
primary motions except lateral bending concluding that coupling patterns occur due to
the anatomy of the osteoligamentous spine, however in lateral flexion the active
structures (muscles) play a key role.
Insertion of Steinman pins into thoracolumbar spinous processes of living subjects has
also been used to assess range of motion (Gregersen & Lucas, 1967) and coupling
(Steffen et al., 1997). Large variations between individuals were noted.
Coupling patterns are reportedly stronger in younger subjects and lateral flexion was
strongly associated with flexion (Russell et al., 1993).
Small amounts of coupling between lateral flexion and axial rotation clearly do occur in
the lumbar spine however the direction remains controversial.
Recent comprehensive reviews of the literature find no clear consensus with respect to
direction of coupling and caution against assumption (Harrison et al., 1998; Legaspi &
Edmond, 2007).
Coupling varies between segments and individuals as well as ex vivo and in vivo
conditions. Further investigation is merited to clarify patterns and the predisposing
factors to each type of motion.
Chapter 2: Review of Literature
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2.1.2.4 The role of the intervertebral disc
The intervertebral disc’s primary function of load attenuation is achieved through the
predominant use of a hydrostatic mechanism (Adams et al., 2002; Adams et al., 1994;
Adams & Hutton, 1983a; Giles & Singer, 1997).
The NP will generally deform towards the convexity in response to offset compressive
loading (Adams et al., 2000; Beattie et al., 1994; Brault et al., 1997; Edmondston et al.,
2000; Fazey et al., 2006; Fennell et al., 1996; Périé et al., 2003; Périé et al., 2001). In a
well hydrated disc this pattern is typically the case however there are exceptions
reported in the literature where deformation occurs towards the concavity (Edmondston
et al., 2000; Fennell et al., 1996).
Most studies examining NP migration in sagittal positioning have supported the theory
that the NP will migrate posteriorly in forward flexion and anteriorly in extension
(Brault et al., 1997; Edmondston et al., 2000; Fazey et al., 2006; Fennell et al., 1996).
These authors have used a variety of methods including visual inspection and
measurement, mapping of pixel intensity and tracking of peak pixel intensity. All have
measured NP migration from sagittal images in that plane alone except Fazey et al
(2006) who measured NP deformation from axial images and in both coronal and
sagittal planes.
These studies examine NP migration, which conceptually must involve measurable
movement of its boundaries within the anulus. While this may be possible within a
compromised anulus, an IVD with an intact inner anulus would contain the NP so as to
allow minimal movement. As such it would be more appropriate to describe this as
representing deformation of the NP. This implies redistribution of fluid content within
an intact anulus in response to compressive force gradients across the disc. Measuring
NP migration alone would potentially not capture deformation and risks overlooking
marked force related change.
It has been reported by Edmondston et al (2000) that occasional individual subjects
exhibit anterior migration in flexion. While this may be due to the discrepancy between
migration and deformation it may also be due to posterior anular tensile forces
exceeding compressive forces anteriorly. This possibility has not been considered in the
literature. Posterior migration in extension would be more easily explained as the
Chapter 2: Review of Literature
Page II-14
posterior elements protect the posterior anulus from excessive compressive force in
extension (Adams et al., 2000).
There is a dearth of literature reporting NP deformation in response to torsion. The sole
report in healthy volunteers was by Fazey et al (2006), where directionality of
deformation was noted to be variable in the coronal plane (Fazey et al., 2006). There has
been limited reporting of NP deformation in the scoliotic spine by Périé (2001, 2003).
Anular bulging is reported to increase anteriorly and decrease posteriorly in flexion
(Adams et al., 2002), however this is challenged in a more recent in vivo MRI study that
reports bulge reduction both anteriorly and posteriorly (Parent et al., 2006b). The former
cites ex vivo studies that include axial loading while the latter reports from in vivo MRI
images obtained in unloaded flexion and extension. This may explain the discrepant
findings. A study employing similar methodology but in an open magnet MRI reported
reduction in posterior bulge on flexion, a finding which supports the ex vivo studies
(Lee et al., 2009).
Intradiscal pressure has been measured during positions such as recumbent lying,
sitting, standing and forward bending (Nachemson, 1960; Wilke et al., 1999). While
limited to primarily sagittal positioning, these studies confirm that pressure increases
occur predictably and in a graded fashion concomitantly with increasingly loaded
postures, from lying through standing and flexion to sitting. Pressures are reduced in
degenerate discs putatively due to the reduced hydrostation (Sato et al., 1999).
Positional anular compressive forces have been measured however not tensile forces.
Controversy exists with respect to pressure changes during in vivo axial rotation. Wilke
et al (1996) reported increased pressure, as did Adams et al (2002), however van
Deursen et al (2001) reported decreased intradiscal pressure in an ex vivo porcine
model, while Yantzer et al (2007) claims no effect. No clear consensus has emerged to
date.
Despite claims that the IVD has self sealing properties it may be that the measurement
technique employing needle pressure transducers interrupts the intradiscal environment
and alters intradiscal pressure unpredictably. This theory is supported by a recent report
Chapter 2: Review of Literature
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of increased incidence of degenerative change in a 10 year follow up of patients having
undergone discography (Carragee et al., 2009). The increased incidence of degeneration
is putatively ascribed to the interruption to the internal disc homeostasis.
Loading the lumbar spine into flexion has been demonstrated to reduce intradiscal fluid
content particularly in the NP (Adams & Hutton, 1983a). This occurs when fluid
transfer occurs through both the peripheral anulus and the central portion of the end-
plate. Simulated diurnal changes in IVD volume have been reported using MRI (Malko
et al., 1999). After sustained loading, subjects demonstrated a mean recovery of 5.4% of
disc volume on supine lying for 3 hours. Volume changes relative to torsion have not
been measured.
Many of the studies on IVD material properties have been conducted ex vivo. This may
explain the variations and inconsistencies. The properties of cadaveric material are
affected by death, cooling and post mortem frozen storage. Despite these changes being
small (Adams et al., 2002) ex vivo studies do not permit exploration of the unknown
physiological variables of a fully functioning organism such as the influence of muscle
function and vascularity.
Recent development of imaging and other techniques capable of accurate in vivo
measurements will ultimately elucidate mechanisms in human volunteers which include
the influences of all relevant physiological systems; muscular, neural, articular and
vascular.
2.1.2.5 Mechanical limits of torsion
The IVD exhibits time-dependent and viscoelastic properties. Sustained loading causes
collagenous tissue to deform over time (creep) accounting for about 25% of disc height
loss. Intervertebral disc creep continues to occur over several hours. Sustained
compressive load has been shown to reduce fluid content of the IVD by 18% in
cadaveric specimens over six hours (McMillan et al., 1996). An in vivo MRI study
reported a 5.4% reduction in total disc volume after three hours of compressive loading
(Malko et al., 1999). In contrast, paraspinal tissues subjected to sustained loading
demonstrate most creep effect in a few minutes (Yahia et al., 1991).
Chapter 2: Review of Literature
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Adjacent anular lamellae are weakly bound and can be pulled apart easily (Schollum et
al., 2008). In the plane of the anulus tensile strength is greater. Small samples in ex vivo
experiments will fail at 1-3 MPa (Adams et al., 2002).
Anular fibres exhibit normal stress strain curves typical of any biological tissue. Early
changes in the stress strain curve have been interpreted as microfailure at 3° of axial
rotation (Farfan et al., 1970). This is now considered to represent straightening of crimp
within anular fibres and failure is reported at much higher ranges (12°) (Bogduk &
Twomey, 1987). Rotational forces may stretch anular fibres by up to 7% (Stokes, 1987).
Deliberate sequential lesioning of facets and unidirectional anular fibres has concluded
that anular fibres are more capable of resisting torsion than the articular facets at lower
torques up to 8.5 Nm (Krismer et al., 1996). At higher torque values resistance by the
facet joints dominate (Adams & Hutton, 1981b). According to Farfan et al (1970)
following facetectomy, anular fibres fail macroscopically at torsion ranges between 11°
and 32°. Other ex vivo studies have noted facet fracture precedes anular rupture (Adams
& Hutton, 1981b).
2.2 Section 2: Degeneration and structural deformity
2.2.1 Degeneration
Considerable literature has been devoted to degeneration of the spine and its various
component parts. The classic paper by Keyes and Compere (1932) and the more recent
studies by Boos et al (2002) provide important reviews. It is beyond the scope of this
thesis to comprehensively review all such literature. Instead, a focus will be directed at
those aspects of degenerative change that influence the IVD’s response to torsion.
2.2.1.1 Morphology
Morphological changes occur progressively in the normal ageing spine. The terms
ageing and degeneration are used interchangeably in the literature and variably given
disease status by the use of the diagnostic term ‘degenerative disc disease’. It could be
argued that normal age related changes should not be considered a disease.
Age changes have been distinguished from degenerative changes by the preservation of
disc height (Twomey & Taylor, 1985).
Chapter 2: Review of Literature
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2.2.1.2 Age changes
Changes attributable to ageing typically commence in the nucleus with a reduction in
proteoglycan production and concentration and therefore hydration. Non enzymatic
glycation causes brown pigmentation of the NP (Figure 2.4B). Cartilaginous endplates
show similar changes (Jensen et al., 2009; Modic & Herfkens, 1990) which may
compromise nutrient supply.
Functionally the NP loses pliancy, volume and hydrostatic capability. Its response to
mechanical stimulus would consequently be altered however there is little examination
of this within the literature relative to torsion.
Figure 2.4: Age changes of the NP. Normal well hydrated NP (A) Glycation causes
brown pigmentation (B) and loss of NP hydration permits inward buckling of anulus (C)
and endplate disruption (D) (Photographs from Adams et al, 2002).
2.2.1.3 Degeneration of the intervertebral disc
Degenerative change of the IVD may occur at any age (Modic & Ross, 2007). While
such change may commence in the second decade of life (Boos et al., 2002; Nerlich et
A
B
C
D
Chapter 2: Review of Literature
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al., 1997) its increased frequency in older discs results in the inevitable linking with
ageing. Age related changes are usually concomitant with gross structural change in the
anulus and end plate and may begin in the nucleus (Haefeli et al., 2006). Anular changes
include radial tears, concentric clefts between lamellae (delamination), buckling of the
inner anulus and rim lesions (Adams et al., 2002).
All of these compromise the intradiscal environment and therefore the ability of the disc
to attenuate load and behave in a predictable manner (Modic & Ross, 2007).
Diffusion changes across the end plate and nucleus have been associated with reduced
nutrition and degenerative disc disease (Rajasekaran et al., 2010; Roberts et al., 1996).
End plate changes include local and generalised sclerosis, irregularity, Schmorls nodes
and bone marrow changes. The latter, or Modic changes, present as types 1, 2 or 3
(Modic & Ross, 2007). Table 2.2 describes the changes observed on T1 and T2
weighted MRI for each type of Modic change. Low signal on T1 weighted images is
associated with inflammation and increased back pain incidence High signal indicates
fatty marrow associated with stability indicating fusion. The relationship between end
plate or marrow signal changes and the response to torsion is unknown.
Modic changes are reported to convert from one type to another and represent different
stages of the same process (Mitra et al., 2004b; Vital et al., 2003; Zhang et al., 2008)
and have been associated with low back pain, degeneration and stability (Luoma et al.,
2009; Modic, 2007; Rahme & Moussa, 2008). Evaluation of Modic changes has
demonstrated good inter tester and excellent intra tester reliability (Fayad et al., 2009;
Peterson et al., 2007a; Zhang et al., 2008).
Table 2.2: Marrow changes on MRI in degenerative disc disease
T1 weighted T2 weighted Marrow status Significance
Type 1 Low (black) High (white) Fibrovascular Back pain, hypermobility
Type 2 High (white) High (white) Fatty Stability
Type 3 Low (black) Low (black) Fibrovascular Back pain, hypermobility
From: Rowe (1997)
Chapter 2: Review of Literature
Page II-19
The literature is consistent with respect to Modic changes and their relationship with
degeneration however there remains controversy over the relationship with low back
symptoms (Jensen et al., 2008; Peterson et al., 2007b; Rahme & Moussa, 2008).
Discs exhibiting degenerative change and radial tears have been shown to contain
granulation tissue and neovascularisation. Accompanying the vascular in-growth are
nociceptive nerve fibres, thereby rendering the degenerate disc more pain sensitive
(Freemont et al., 1997). Discogenic pain has been postulated to be linked to damage to
the outer anulus (Fraser et al., 1993) consistent with its innervation being largely
nociceptive (Fagan et al., 2003). Induced tears of the anular periphery may precipitate
degenerative changes involving the entire intervertebral disc (Osti et al., 1990). A model
of disc degeneration incorporating causative factors and changes at molecular,
microscopic and macroscopic levels, and as displayed by imaging has been proposed
(Figure 2.5) (Hadjipavlou et al., 2008).
Increased ranges of segmental axial rotation in the lumbar spine have been linked with
degenerative change (Haughton et al., 2002) and concordant pain on discography
(Blankenbaker et al., 2006). Rohlman (2006) using finite element modeling, reported
increased axial rotation range in mild degeneration but decreased ranges in more
severely degenerated discs (Rohlmann et al., 2006).
2.2.2 Structural deformity involving the intervertebral disc
The most common structural spinal deformity that includes a rotational component is
scoliosis. The pathogenesis of scoliosis is unknown though likely to be multifactorial
(Kouwenhoven & Castelein, 2008). There are numerous classifications of scoliosis, the
most common being idiopathic (Reamy & Slakey, 2001). The deformity is tri-
dimensional with changes in coronal, axial and sagittal planes (Wright, 2000). While
deformity was traditionally assessed from plain Xray the advent of axial imaging has
sparked interest in the axial rotation component (Kuklo et al., 2005). The rotational
component has a demonstrated association with the coronal deformity as the degree of
segmental rotation can predict coronal imbalance postoperatively (Behensky et al.,
2007). This is reasonable given the existence of coupled motion in the spine, however
segmental axial rotation has been demonstrated not to be altered by lateral flexion as it
would in the normal spine (Beuerlein et al., 2003). The rotational deformity occurs in
Chapter 2: Review of Literature
Page II-20
both the disc (55%) and the vertebral body (45%) (Birchall et al., 2005; Liljenqvist et
al., 2002).
Anulus Fibrosus Nucleus Pulposus Vertebral Endplate
Molecular cross-linking altered PGs
altered pH
dehydration
altered PGs
Microscopic Delamination, tears,
fissures, Fibrosus
Cracks, tears,
fractures
Thickening, cracks
Biomechanical Stiffening, increased
stress
depressurised Weakening, bowing
Imaging osteophytes Reduced signal
Figure 2.5: A simple model of disc degeneration. Multiple causative influences
interrupt the balance between synthesis and degradation of the matrix and are expressed
as features at molecular, microscopic and biomechanical levels
(From: Hadjipavlou et al, 2008).
Ageing Genetics Nutrition Metabolic Infection Mechanical
Degradation Synthesis
Matrix
Chondrocyte
Chapter 2: Review of Literature
Page II-21
2.3 Section 3: Imaging and measurement
2.3.1 History of spinal imaging
Since the discovery of Xrays in 1895 there have been many advances in technology and
technique to refine the diagnostic capabilities of musculoskeletal imaging. Introduction
of water based contrast in 1963 led to myelogram and the ability to image neural
structures in the spine (Sofka & Pavlov, 2009). The advent of cross sectional imaging –
Computerised Tomography (CT), Magnetic Resonance Imaging (MRI) and
Ultrasonography (US) – has made visualization of exquisite anatomic detail possible.
Clinicians now have at their disposal an array of options for imaging the spine including
plain Xray, discography, myelography, CT and CT myelography, MRI and nuclear
scintigraphy.
The literature has varied recommendations for the use of imaging, from being
mandatory for a patient with a suspected disc lesion (DePalma & Rothman, 1970) to
only if the results obtained will change treatment (Boden, 1996). False positives and
false negatives are common as imaging alone cannot identify a pain generating
structure. Provocative discography is the putative exception though this has also been
challenged (Carragee & Alamin, 2001; Carragee et al., 2009; Feydy et al., 2009).
2.3.2 Imaging types and their limitations
2.3.2.1 Plain Xray
Each type of spinal imaging has its uses and limitations. Plain radiographs have limited
value beyond identification of overt bony injury or deformity (Sofka & Pavlov, 2009;
Wright, 2000). Observation of changes in adjacent structures may allow an indirect
assessment for example, reduction in disc space and osteophytosis is reported to infer
disc degeneration although direct visualization of the disc is not possible (Malfair &
Beall, 2007).
2.3.2.2 Stereoradiography
Stereoradiography is used primarily for motion analysis in two planes and was popular
in the 1980s (Dvorak et al., 1991; Pearcy et al., 1984; Pearcy & Tibrewal, 1984). Recent
use has been in digital form for 3 dimensional reconstruction (Rousseau et al., 2007).
Chapter 2: Review of Literature
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2.3.2.3 Computerised Tomography (CT)
While CT visualizes soft tissue, neural structures and IVD more clearly, especially
when performed with the addition of contrast, it remains insensitive to early
degenerative changes (Malfair & Beall, 2007). Computerised Tomography also has the
ability to generate 3 dimensional images of bony structures. Anular tears may also be
identified on CT when combined with discography, reportedly with greater accuracy
than with MRI. In particular circumferential tears are better visualized with contrast CT
than discogram as they are not continuous with the nucleus pulposus (Kluner et al.,
2006).
2.3.2.4 Diagnostic Ultrasound
There is little support in the literature for the routine use of ultrasonography in imaging
the spine (Tan et al., 2003). It is potentially of some use in assessing paraspinal
structures and measuring cross sectional area of muscle (Hides et al., 2008a) and
enthesitis (D'Agostino et al., 2003).
2.3.2.5 Magnetic Resonance Imaging
There is little disagreement in the literature that MRI and its various modifications have
superseded most other forms of imaging of the spine (Dudler & Balague, 2002). Its
multiplanar ability to accurately image anatomy and its sensitivity to subtle change in
fluid makes it the method of choice from which to assess such changes as IVD
degeneration, herniated NP, bone marrow oedema, inflammation and soft tissue
swelling (Lamminen, 1990; Lamminen et al., 1990; Luoma et al., 2009; Luoma et al.,
2001; Malko et al., 1999; Tan et al., 2003).
MRI has high sensitivity and specificity in detecting disc herniation (Moon et al., 2009),
disc height variations (Boos et al., 1996) and anular tears (Milette et al., 1999).
T2 relaxometry has the important ability to identify free water in the disc which is
known to vary with ageing and degeneration. Changes in total disc volume on MRI
have been used to analyse diurnal changes in fluid content (Malko et al., 1999).
Areas of high intensity on T2 weighted images, while somewhat controversial
(Carragee et al., 2000a; Mitra et al., 2004a; Park et al., 2007; Rankine, 2004), have been
correlated with anular tears and concordant pain (Aprill & Bogduk, 1992; Lam et al.,
2000; Lim et al., 2005). These studies employed discography to determine concordance.
One investigation performed a histological examination post operatively and concluded
Chapter 2: Review of Literature
Page II-23
that high intensity zones contained vascularised granulation tissue extending into the NP
(Peng et al., 2006a; Peng et al., 2006b).
2.3.3 Imaging the intervertebral disc
The IVD can be directly visualized with CT, MRI and discography. These modalities
can be used in isolation or combination, with or without contrast medium.
CT can identify disc herniation and anular tears. The addition of contrast allows better
identification of anular tears. MRI also clearly depicts anular tears. Its ability to show
subtle hydration changes, inferred from signal intensity, gives accurate information
regarding degeneration staging (Modic & Ross, 2007; Pfirrmann, 2006).
2.3.3.1 Discography
The introduction of contrast medium to the IVD prior to imaging (discography) has
been considered the gold standard in imaging internal disc disruption and anular tears
(Sofka & Pavlov, 2009) and has been reported as more accurate than MRI in detecting
anulus pathology (Osti & Fraser, 1992). Concomitant provocation of concordant
symptoms during discography has been assumed to enhance its clinical utility in
identification of symptomatic discs however, discography remains a poor predictor of
surgical outcomes (Saboeiro, 2009) with questionable diagnostic value (Kluner et al.,
2006).
The ability of provocative discography to accurately identify disc source of pain has
been questioned (Holt, 1968). Morphological changes within the disc did not correlate
well with painful discs (Ito et al., 1998).
Numerous other studies have reported poor positive predictive value (Walsh et al.,
1990) and an unacceptable rate of false positives (Carragee et al., 2000b).
Carragee (2001) found that concordant pain could be reproduced via discography in
patients with a known non spinal symptomatic source; bone graft donor site pain at the
iliac crest was reproduced on discography (Carragee & Alamin, 2001).
Anular disruption evidenced on discography is a weak predictor of future low back pain
(Carragee et al., 2004).
However, Manchikanti (2009) in a more recent systematic review found that, with strict
adherence to protocols, lumbar discography remained a useful tool in evaluation of
chronic lumbar discogenic pain (Manchikanti et al., 2009).
Chapter 2: Review of Literature
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Discography alone clearly has questionable diagnostic ability, however it can help
resolve discordance between imaging and clinical findings (Kluner et al., 2006).
Judicious use is recommended as a 10 year matched cohort study by Carragee et al
(2009) linked discography with accelerated rates of degeneration, disc herniation and
reduced disc signal on MRI.
2.3.4 Imaging the nucleus pulposus (NP)
Imaging the NP allows inferences to be made as to physiological, morphological and
putative positional changes of the NP within the IVD.
Apart from discography which, along with anular defects, can highlight the NP, MRI is
the only imaging modality that confers such information to the examiner (Haughton,
2004).
Signal strength from T2 weighted images infers the degree of hydration and, by
extension, potential degenerative change and reduction in proteoglycan content
(Haughton, 2006).
Few studies report morphological or behavioural changes specific to the NP, rather the
majority focus on anular disruption as indicated by failure of NP containment.
Several studies have examined putative NP positional change following changes in
sagittal plane position, using a variety of measurement methods based on T2 weighted
sagittal images (Alexander et al., 2007; Beattie et al., 1994; Brault et al., 1997;
Edmondston et al., 2000; Fennell et al., 1996).
Three dimensional modeling of NP deformation in scoliosis using image processing
software has also been reported (Périé et al., 2001) and correlated with the degree of
deformity (Périé et al., 2003). To date this is the only examination of NP deformation in
planes other than sagittal.
2.3.4.1 Diffusion weighted MRI
Diffusion weighted MRI was originally developed as a tool for early identification of
cerebral ischaemic lesions (Fisher et al., 1992). It uses T2 weighted images to measure
the relative amount of water diffusion (Haughton, 2006). More recently it has been used
to measure water diffusion within and across selected tissues including the IVD (Kealey
et al., 2005; Kerttula et al., 2000).
This technique has been subsequently reported as a reliable method to measure fluid
diffusion in the NP following physical therapy intervention with sagittal plane exercise
Chapter 2: Review of Literature
Page II-25
and positioning (Beattie et al., 2010; Beattie et al., 2008). To date this method has not
been tested for sensitivity to differential hydration patterns within the NP.
2.3.5 Quantification of spinal motion and pathology
2.3.5.1 Herniated nucleus pulposus (HNP)
There is much literature describing herniated nucleus pulposus (Kim et al., 2009; Moore
et al., 1996; Parisien & Ball, 1998; Scannell & McGill, 2009) and its natural history to
resorb over time (Atlas et al., 2005; Autio et al., 2006; Benoist, 2002; Cribb et al., 2007;
Kobayashi et al., 2003; Singer et al., 2004). Quantification of the HNP is typically via
linear measurement of the herniated portion (Cribb et al., 2007; Parent et al., 2006a),
linear measurement of the thecal sac or cross sectional area of the thecal sac. These
methods are all considered reliable and linear thecal sac dimensions are reported to
correlate well with cross sectional area (Pneumaticos et al., 2000).
2.3.5.2 Fat infiltration into paraspinal musculature
It has been noted that morphological and histochemical changes occur in muscle
following injury or disease and present as fat infiltration (Yoshihara et al., 2001; Zhao
et al., 2000). This phenomenon has also been reported in association with a variety of
spinal conditions including whiplash associated disorders (Elliott et al., 2006; Elliott et
al., 2008; Elliott et al., 2005) and Duchenne Muscular Dystrophy (Kjaer et al., 2007;
Mengiardi et al., 2006). Fat inflitration has been measured in various ways including
calculation of a muscle/fat index from T1 MRI (Cagnie et al., 2009) and digital image
analysis (Lee et al., 2008). Elliot described a reliable method of comparison by image
analysis of isolated pixel intensities in both muscle and fat from which a percentage of
each can be derived in a select muscle sample (Elliott et al., 2005). A limitation of these
cross sectional studies is their inability to predict changes over time.
2.3.5.3 Muscle cross sectional area
Cross sectional area of muscle has been used to quantify trophic changes. Numerous
studies have employed this measure in analysis of trunk and peripheral muscle injury
using image analysis software (Barker et al., 2004; Herlidou et al., 1999; Hides et al.,
2008b; Kader et al., 2000; Kang et al., 2007; Kjaer et al., 1173; Messineo et al., 1998;
Phoenix et al., 1996). While both ultrasound (Hides et al., 1996) and T1 weighted
magnetic resonance images (Hides et al., 2007) have been used, the majority have
Chapter 2: Review of Literature
Page II-26
preferred MRI. Ultrasound based analysis has been reported comparable to MRI
analysis with adherence to strict protocols (Khoury et al., 2008; Stokes et al., 2005)
however clearer visualization of tissue planes on MRI would generally confer greater
accuracy.
2.3.5.4 Measuring segmental axial rotation in the lumbar spine
The first in vivo measurements were reported following insertion of Steinman pins into
the lumbar spinous processes of volunteer subjects (Gregersen & Lucas, 1967).
Subsequent studies have employed techniques such as stereoradiography (Pearcy &
Hindle, 1991a; Pearcy et al., 1984; Pearcy & Tibrewal, 1984) computerized MRI
analysis (Haughton et al., 2002) or CT (Blankenbaker et al., 2006; Singer et al., 2001;
Singer et al., 1989).
Segmental rotation has been measured in idiopathic scoliosis with three dimensional
MRI analysis (Birchall et al., 2005; Birchall et al., 1997) and multiplanar reconstruction
(Liljenqvist et al., 2002). Typically these methods all involve mathematical calculation
of axial plane motion using specific image points or anatomical landmarks on the
adjacent segment. Segmental axial rotation measurement using a variety of techniques
has been prone to observer error (Vrtovec et al., 2009).
Vrtovec has summarized the literature relevant to both two and three dimensional
analysis of segmental rotation (Vrtovec et al., 2010). However, this review
predominantly cites literature relative to scoliosis and neglects earlier two dimensional
in vivo studies (see section 2.1.2.1) or those that relate axial rotation range to
degenerative change (see section 2.2.1.3). These contributions have used a variety of
measurement techniques including stereoradiography (Pearcy & Tibrewal, 1984), twist
CT scans (Singer et al., 2001) and Steinmann pins plus either a protractor (Gunzburg et
al., 1991) or Fastrak motion analysis (Steffen et al., 1997).
2.4 Summary
This chapter has reviewed the literature relevant to the anatomy, physiological
mechanisms, biomechanics and pathology of the lumbar intervertebral disc. The
emphasis has been on aspects of those topics pertinent to torsion, consistent with the
thesis focus on mechanistic studies rather than broader epidemiological surveys. Clearly
there are anatomical and functional features that are torsion specific and the literature
Chapter 2: Review of Literature
Page II-27
has reported these to an extent. The literature relevant to imaging techniques employed
in investigation of the IVD has been reviewed, with emphasis on those used in the
investigations of this thesis.
This review highlights that there is limited literature examining lumbar rotation
mechanics. Although more recent studies have examined positional effects on the NP
there remains a paucity of data specific to the NP and its response to torsion. An
omission from the literature is the mapping of hydration pattern changes relative to axial
plane position. While reports exist of unidimensional hydration changes relative to
sagittal plane positioning from single pixel width samples, there are none reporting
biplanar changes with axial rotation positional change. Axial and coronal plane motion
are coupled physiologically necessitating measurement of changes in both planes in
order to accurately evaluate the relative contribution of each to observed hydration
change.
A thorough consideration of this question would require age contrasting, as IVD
hydration changes with age. Investigation should also extend to spinal deformity in
scoliosis where both axial and coronal plane deformity occur in tandem.
Another deficit in the literature is a longitudinal study of changes associated with
rotational disc injury. This should include quantification of changes in paraspinal tissues
relative to IVD changes over time.
Chapter 2: Review of Literature
Page II-28
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CHAPTER 3
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Methods
3.1 Overview
This chapter describes the methods used in the subsequent chapters and the rationale
underpinning their modification through the development of both the hypotheses and
the thesis. Additionally the influences that informed those changes in method will be
explained.
3.2 Research Design
The studies forming chapters in this thesis use a mix of research designs.
The MRI based studies presented in chapters 5,6,7 and Appendix 4 are observational
cohort studies. Chapter 8 is a retrospective cohort study and chapter 9 a retrospective
longitudinal case study.
3.3 Research Hypotheses
3.3.1 Chapter 4: The ex vivo CT study
The objective of this study was to examine the influence of lumbar zygapophysial joint
anatomy and intervertebral disc pathology on axial torsion response in ex-vivo
ligamentous lumbar spine preparations using 3D motion tracking and computed
tomography (CT). Segmental rotation and zygapophysial joint separation trends were
compared to radiographic evidence of joint orientation and macroscopic evidence of
disc degeneration.
This preliminary study focussed on zygapophysial joint geometry and orientation, and
stage of disc degeneration. Consequently an interest was given to the response within
the internal disc environment, specifically of the lumbar NP, to rotation.
In order to investigate this, a hypothesis was generated that sagittal and axial plane
positions would induce a directionally predictable deformation of the NP. Additionally,
the unknown influence of conjunct coronal plane position was assessed. To investigate
this hypothesis a novel series of studies using MRI was developed.
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3.3.2 The pilot study (Appendix 1)
The aim of this study was to assess a novel method using MRI to track NP deformation
in response to flexion and extension positions, and the combined positions of flexion
with left rotation and extension with left rotation, at L1-2 and L4-5.
3.3.3 The normative cohort MRI study (chapter 5)
This study adopted the method from the pilot study with minor refinement and applied
it to a larger group of young normal subjects to test the hypothesis that NP deformation
resulting from sagittal, axial and conjunct coronal plane segmental positions would
occur predictably towards the convexity. Additionally, any relationship between axial
rotation direction and NP deformation direction would be determined.
3.3.4 The lateral flexion cohort MRI study (chapter 6)
This study sought to assess the effect of coronal plane positioning alone on NP
deformation. This tested the hypothesis that the NP would deform predictably towards
the convexity and with a magnitude proportional to the range of segmental lateral
flexion.
3.3.5 The aged cohort MRI study (chapter 7)
With minor refinement of method, older subjects with signs of lumbar disc degeneration
were assessed with MRI to test the hypotheses that greater segment lateral flexion
would induce the largest NP deformation from the neutral position; that more severe
disc degeneration would reduce the extent of NP deformation following axial or coronal
plane positioning and that the NP would deform contralaterally to the direction of
segmental lateral flexion.
3.3.6 The scoliosis cohort MRI study (chapter 8)
Scoliosis is the primary spinal condition that includes deformity in both axial and
coronal planes. A retrospective observational cohort study was undertaken to test the
hypothesis that in lumbar compensatory scoliotic curves, NP deformation magnitude at
the apex of the curve would be associated with the extent of intersegmental lateral
flexion range.
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3.3.7 The IVD herniation longitudinal case study (chapter 9)
This 12 year retrospective longitudinal single case study followed the natural history of
a rotation injury to the IVD by serial assessment of herniation size, paravertebral muscle
cross sectional area and degree of fat infiltration. It tested the hypothesis that restoration
in paravertabral muscle size and composition occur with normal activity after 12 years.
3.4 Subject Recruitment
3.4.1 Normative and aged cohort studies
Subjects for the MRI studies reported in chapters 5,6,7 and Appendix 4 were selected
from community volunteers including post graduate students at The University of
Western Australia. Approval was obtained from an institutional ethics committee
[Royal Perth Hospital EC2003-101] (Appendix 1) and written consent obtained from
the subjects (Appendix 2, 3).
Inclusion criteria were:
a) Age consistent with the defined range for each study
b) No history of significant low back pain requiring intervention over the past year
c) No contraindications to MRI
Exclusion criteria were:
a) Current or previous low back pain requiring intervention in the preceding year
b) Presence of any contraindication to MRI
a. Any ferromagnetic implants
b. Any implanted mechanical device
c. Intraorbital metal fragments
d. Claustrophobia
e. Pregnancy
3.4.2 Scoliosis cohort MRI study
Cases for this retrospective study were selected following an audit of patients presenting
to the scoliosis clinic at Royal Perth Hospital and listed for corrective surgery between
July 2007 and April 2011. Subjects (n=14) were selected from an inclusive list of all
patients of three spinal deformity surgeons (PW, EM and DD) requiring pre-operative
MRI evaluation to exclude occult neurological pathology (n=113).
Inclusion criteria were MRI evidence of:
a) Secondary lumbar curvature
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b) Availability of mid disc axial T2 weighted images through the apical segment of
the lumbar curve
c) Availability of T1 weighted coronal images through the apex of the lumbar
curve
d) Availability of regional coronal lumbar plain radiographs for measurement of
lumbar Cobb angles
Exclusion criteria were
a) no secondary lumbar curvature
b) incomplete image sequences
3.4.3 IVD herniation longitudinal case study
The subject for this longitudinal single case study was identified, on request, by a
consultant spinal surgeon (PW). Historical imaging was accessed from records in hard
and electronic format. The subject was contacted to seek consent and requested to
present for subsequent MRI assessment by the consultant surgeon for scheduled re
evaluation. Routine written consent for MRI was obtained (Appendix 3).
3.5 Imaging positions and parameters
3.5.1 Ex vivo CT study
Three post mortem human thoracolumbar spines were obtained. Each was positioned in
a purpose built torsion apparatus. A 3Space® FastrakTM
(Polhemus, Vermont, USA)
electromagnetic motion tracking device was used to measure the segmental
displacements occurring in the specimens via sensors attached to the vertebral bodies.
Following a period of pre loading, rotation to right and left was induced in various
sagittal plane positions. The protocol was repeated within a CT imager (Siemans:
Tomoscan, Berlin, Germany) and images obtained in each position.
3.5.2 The pilot and normative cohort MRI studies
Positioning and scanning parameters were identical for both studies. Each subject was
initially positioned supine on the gantry of 1.5T MR imager (Siemens, Berlin,
Germany). A cylindrical roll of towel was placed under the lordosis to extend the
lumbar spine. T1 weighted localizer sagittal and coronal images (TR/TE [24/6], field of
view 400mm, 512x512 matrix) and T2 weighted axial images (TR/TE [5160/102], field
of view 210mm, 384x384 matrix) were acquired with a fast spin echo sequence, slice
Chapter 3: Methods
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width 4mm. Target segments were L1-2 and L4-5. The subject was then repositioned
into extension plus left trunk rotation by the placement of a dense foam wedge cushion
under the left hemipelvis and image sequences repeated.
Lumbar spine flexion positioning prior to image acquisition was achieved by placement
of wedge cushioning under the sacrum and thorax with pillows to support the flexed
cervical spine and knees. Left trunk rotation in flexion was induced by the placement of
a dense foam wedge under the left hemipelvis in the flexed position.
Figure 3.1: Subject positioning on the MRI gantry into lumbar extension (A) and
lumbar flexion (B). [Image reproduced with permission from Clinical Biomechanics
2006, 21 (538-542)].
This investigations were preliminary, then exploratory. Selection of unilateral trunk
rotation reflected an attempt to minimise cost and time within the magnet, and the
potential discomfort associated with sustained positioning within the MRI. The choice
of left over right trunk rotation was arbitrary. The same method was adopted for
consistency, with respect to subjects’ trunk rotation direction across the studies
described in chapters 5, 7 and Appendix 4.
A
B
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3.5.3 The lateral flexion cohort MRI study
As preliminary results indicated that conjunct lateral flexion induced more directionally
predictable NP deformation, a study with specific primary positioning into lateral
flexion was conducted.
Scanning was extended to include all lumbar segments and intervening IVDs.
Each subject was initially positioned supine on the gantry of a 0.2T horizontally open
MRI unit (AIRIS mate, Hitachi Inc., Sopporo, Japan). The gantry was inserted into the
magnet and a series of T1 and T2 weighted images acquired in both the supine neutral
and laterally flexed position.
The neutral axial T2 weighted images were acquired through the mid disc region from
L1-2 to L5-S1 with a fast spin echo sequence (3120/120 [TR/TE], FOV 260) 8mm slice
thickness and an acquisition time of 6:52 min.
The pelvis was then stabilised with a strap to prevent rotation and the subject was
positioned into left side bending with one assistant manually holding the legs at the
level of the knees to prevent lateral movement. The subject was then asked to actively
laterally flex to the limit of their range. A second assistant applied overpressure via the
shoulders to minimise trunk rotation and to achieve a limit of passive lateral flexion
range, which was maintained passively by the assistants during imaging. Mid disc
image sequences at all levels were repeated using the same parameters.
Additionally, axial T1 weighted images were taken through the bony vertebra of L1 to
S1 using a fast spin echo sequence (385/24.5 [TR/TE], FOV 300) slice thickness 6mm,
acquisition time 5:45 min and coronal T1 images (285/24.5 [TR/TE], FOV 300) 6mm
thickness, 1:34 min to evaluate segmental rotation and lateral flexion respectively.
3.5.4 The aged cohort MRI study
The normative and lateral flexion studies helped identify the issue of coronal slice angle
influence on segmental lateral flexion measurements. In the rotated position, coronal
slices, used to evaluate intersegmental lateral flexion range and direction, may partially
capture regional sagittal curve (Figure 3.2). Coronal slices orthogonal to the axial plane
position for each candidate level were therefore acquired.
Subject positioning was limited to neutral and left trunk rotation to eliminate potential
influence of biplanar positioning on NP deformation direction and range.
Chapter 3: Methods
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Subjects were positioned on the gantry of a 1.5T MRI unit (Siemens, Berlin, Germany)
in the supine and left rotated positions. A series of T2 weighted axial and T1 coronal
images were acquired.
Figure 3.2: Coronal image slices parallel to the MRI gantry (A,p) in a rotated lumbar
spine may be influenced by sagittal curvature (B). Image slice angle orthogonal to the
rotated segment position (A,o) captures coronal plane positional change.
Axial T2 weighted neutral images were obtained through the mid disc region from L1 –
2 to L5 – S1 using a fast spin echo sequence (TR/TE [3020/102.0], field of view
20.9x16.7cm, 306x384 matrix, 4mm slice thickness).
Coronal T1 weighted images were also obtained at each candidate level with a fast spin
echo sequence (TR/TE [619.0/11.0], field of view 30x30cm, 448x448 matrix 4mm slice
thickness). The coronal slices were oriented orthogonal to the axial position for each
imaged level.
Following acquisition in the neutral position the subjects were repositioned into left
trunk rotation by the placement of a dense foam cushion wedge under the left
hemipelvis and image sequences repeated.
A B
p
o
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3.5.5 The retrospective studies: The scoliosis cohort and longitudinal case studies
Subjects for these studies (described in chapters 8 and 9) had undergone routine
imaging with standard T1 coronal and T2 weighted axial sequencing for MRI in neutral
supine positioning. Additionally, erect P-A radiographs were obtained for all subjects in
the scoliosis study (chapter 8).
3.6 Image analysis
3.6.1 The Ex vivo CT study
CT films obtained were video-digitised, scaled and analysed for zygapophysial joint
angles and separation using image analysis software from the National Institute of
Health, Bethesda, USA (NIH Image, 1.58). Degree of disc degeneration was
subsequently assessed directly from mid-axial slices cut from each disc.
Following all motion studies the medial and lateral margins of the superior articular
facets were marked to determine the joint space length. From the mid point of this line,
2/3 of the joint space was divided into regions. The separation of the joint for each
region was measured and the average separation of the articular surfaces calculated.
3.6.2 The MRI studies of NP deformation and rotation
Image analysis in all MRI studies, with the exception of that in chapter 9, was
undertaken with Image-J software (NIH, Bethesda, USA). Parameters analysed
included: pixel intensity profiles, segmental lateral flexion and axial rotation angles.
3.6.2.1 Pixel profiles of the intervertebral disc to assess hydration
The pilot study (Appendix 1) tracked movement of the peak pixel point which was
assumed to represent direction and magnitude of fluid shift within the IVD. This
method had been used by other authors (Alexander et al., 2007; Brault et al., 1997;
Edmondston et al., 2000); all taking single line samples across sagittal T2 weighted
images. Pixel sampling in the pilot study was derived from mid disc T2 weighted axial
images across which 3 equidistant lines were placed from right to left and anterior to
posterior. Raw pixel intensity data from these lines were normalised to 100 points,
averaged using a Labview software routine (National Instruments, Austin, USA), then
imported into Excel where the direction and magnitude was derived (Figure 3.3).
Chapter 3: Methods
Page III-9
Figure 3.3: Pixel data from equidistant samples lines in A-P and lateral directions
across axial T2 weighted images (A) were normalised to 100 points and averaged in a
labview routine (B).
Averaged data from three line samples was considered more representative of hydration
profile than a single line sample. Axial images were considered to capture the broad
distribution of hydration signal better than sagittal images. The basis for using axial
images was the presumption that it would sample more of the disc. All studies used
4mm slice thicknesses from which pixel profiles were derived. Given that lateral and
height dimensions of the disc being, on average, 56mm and 11mm respectively
(Gocmen-Mas et al., 2010), a 4mm sample would represent 7.1% of the disc through the
sagittal plane and 36.4% through the axial plane. With the hydration signal being non
uniform the smaller the sample as a percentage the less representative it would be of the
general trend.
The only exception to this method was the study in the lateral flexion cohort study
(chapter 6) where 6mm slice thickness was used.
Graphic three dimensional representation of hydration signal highlighted the variability
of hydration signal across the disc (Figure 3.4A). Graphs of averaged data also
identified multiple peaks of pixel intensity (Figure 3.4B). The assumption that peak
pixel point movement best represented the total hydration shift was consequently
questioned.
A B
Chapter 3: Methods
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Figure 3.4: Three dimensional representation of signal strength highlights the
variability of hydration distribution (A). Multiple peaks of maximum hydration points
(arrows) in each sample (B) question the validity of these as accurate representations of
total hydration weighting. Subsequently, area under the curve of each half of the pixel
plot was adopted to derive the percentage weighting.
In order to better capture the weighting of fluid shift subsequent analysis compared total
raw pixel numbers under each half of the averaged data plot to derive a percentage
change in weighting between data from neutral and rotated positions. This was
considered more representative than the movement of a single pixel peak point.
Previous authors used the terminology NP migration creating an concept of movement
of the NP within the anulus. In an intact anulus NP movement is confined and
minimised by the inner capsular fibres. This does not prevent a marked redistribution of
fluid within the confines of the anulus which is captured by the use of all available pixel
numbers under the curve.
Reliability assessment using coefficient of variation for this method on multiple image
samples was consistently <4%.
3.6.2.2 Angle measurements
Angle measurements of segmental rotation, lateral flexion and lumbar Cobb in the
sagittal and coronal planes, were used in the studies from chapters 5 though 8. All
angles were measured within image analysis software Image J.
A B
39 % 61%
Chapter 3: Methods
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Segmental rotation (θ) was derived from the angle subtended by a line drawn through
mid disc/vertebral body point and the interlaminar point and the image border (Figure
3.5A). This was subtracted from the angle calculated at the subjacent segment to
determine intersegmental range.
Figure 3.5: Segmental rotation angle (θ) was derived by creating an angle between the
the image border and a line through the mid disc and interlaminar points (A).
Intersegmental lateral flexion angles (Ø) were derived from the angle subtended by the
intersection of lines extended from the inferior endplate of one vertebra and the superior
endplate of the subjacent vertebra (B).
Intersegmental lateral flexion (Ø) was measured from coronal T1 weighted images upon
which a line of best fit was placed across endplates adjacent to an IVD (Figure 3.5B).
The angle of intersection was measured as the intersegmental lateral flexion angle.
The lateral flexion cohort study (chapter 6) uses a minor modification to this method as
the lateral flexion angle is measured from the intersection of two lines through the mid
points of lines joining vertebral body corners (cf: chapter 6, Figure 6.2B).
Cobb angles to measure lumbar regional curvature in the sagittal and coronal planes in
the lateral flexion and scoliosis studies respectively, were derived using the method
described by Cobb (1948). Lines were placed along the superior and inferior end plates
of the upper and lower most vertebra in the curve respectively. The angle subtended by
orthogonal lines extending from each was taken as the Cobb angle.
θ
Ø
A B
Chapter 3: Methods
Page III-12
3.6.3 The longitudinal case study
This study evaluated lateral and A-P thecal sac dimensions, multifidus cross sectional
area (CSA) and fat infiltration. All data were derived using image analysis software,
Image-J (NIH, Bethesda, USA), calibrated for millmetre (mm) unit measure for all
linear and CSA measurements from the respective image scale markers.
3.6.3.1 Areal and linear measuements
Linear thecal sac dimensions were measured by placing lines across the thecal sac in
both coronal and sagittal planes at points of maximal diameter determined by visual
inspection. Cross sectional area required the outlining of the region of interest (ROI).
Care was taken to exclude intermuscular fat and fascia. Area values in mm were
calculated within Image-J.
3.6.3.2 Fat infiltration of multifidus
The percentage fat infiltration of multifidus was derived from T1 weighted axial images
using a consistent circular region of interest (ROI) identified within muscle tissue of
multifidus, with care to avoid any intermuscular or intramuscular fat. From this region a
histogram of pixel values was produced via Image J which reported maximum and
minimum values (Figure 3.6A).
The same ROI was then positioned into adjacent subcutaneous fat, with care to ensure
the ROI area was unchanged, and a second histogram of pixel values produced (Figure
3.6B).
The mid point between the highest pixel value for muscle and the lowest pixel value for
fat was taken as a cut off point to delineate pixels attributable to fat vs muscle signal.
Finally, the entire area of multifidus was outlined as the ROI as described previously
and a histogram produced (Figure 3.6C).
Raw pixel data from the histogram were imported into Excel where the cut off point
was applied. Raw pixel numbers pertinent to fat and muscle were then derived. The data
for fat was converted to a percentage of the pixel numbers for the entire ROI.
Chapter 3: Methods
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A
B
C
Figure 3.6 Regions of interest (outlined in yellow) were identified in muscle (A),
subcutaneous fat (B) and multifidus (C). Histograms of pixel data were produced from
each.
3.7 Statistical analysis
Descriptive statistics were used throughout. Reliability of measures was determined by
Coefficient of Variation (CV).
Chapter 3: Methods
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Angular measurements were all considered to show acceptable reliability with CVs
<3% and NP deformation percentage <4% from repeated measures of representative
images.
Pearson’s correlation coefficient was used to determine associations between variables
where appropriate, in particular that of NP deformation and segmental angular measures
in coronal and axial planes.
For all tests of statistical significance a probability of p<0.05 was taken to represent
meaningful differences.
Chapter 3: Methods
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References
Alexander LA, Hancock E, Agouris I, Smith FW, MacSween A. The response of the
nucleus pulposus of the lumbar intervertebral discs to functionally loaded
positions. Spine 2007; 32(14): 1508-12.
Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar
intradiscal deformation during flexion and extension by mathematical analysis
of magnetic resonance imaging pixel intensity profiles. Spine 1997; 22: 2066-
72.
Cobb J. Outline for the study of scoliosis. American Academy of Orthopaedic Surgeons.
Instructional Course Lectures 1948; 5: 261-75.
Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,
Singer K. MRI evaluation of lumbar spine flexion and extension in
asymptomatic individuals. Manual Therapy 2000; 5: 158-64.
Gocmen-Mas N, Karabekir H, Ertekin T, Edizer M, Canan Y, Duyar I. Evaluation of
Lumbar Vertebral Body and Disc: A Stereological Morphometric Study.
International Journal of Morphology 2010; 28(3): 841-7.
CHAPTER 4
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The ex vivo CT study
4.1 Summary
Spinal motion assessment provides insight into the mechanical response of the mobile
segments and is important in the assessment of spinal instability. Radiological and
laboratory investigations have been limited by the complexities of recording rotation
motion which arise when the spine is deformed by torsion. Specifically, there have been
comparatively few investigations into the influence of zygapophysial joint and disc
degeneration on segmental axial plane motion in the lumbar spine.
A torsion apparatus was constructed to induce torsional loading in three ligamentous
lumbar spine preparations. Rotation displacements were recorded first with a Fastrak
3D motion tracking device to assess the effect of load increments in: neutral, flexion
and extension positions. Zygapophysial joint morphology was examined using a CT
protocol to relate macroscopic evidence of disc and facet joint degeneration to each
segment’s response to torsion.
Marked individual variation in both stage of disc and facet degeneration and
geometrical configuration of the zygapophysial joints was observed. Axial rotation and
joint separation was greatest for the lower lumbar segments which corresponded with
more coronal joint angles. Slight flexion generally resulted in increased segmental
rotation compared with neutral and extension positions, except in the presence of
marked segmental degeneration. The case with the most advanced disc degeneration
showed the greatest axial rotation and separation responses.
Separation of the zygapophysial joint is a normal response during axial rotation
movements. However, anatomical configuration of the paired zygapophysial joints, and
the stage of degenerative disc disease impacts on segmental mobility.
Chapter 4: The Ex vivo CT study
Page IV-2
4.2 Introduction
Factors influencing spinal segmental motion include the anatomical configuration of the
bony elements, compliance of non contractile soft tissue structures including the
intervertebral disc (IVD) and the active stabilizing function of muscles (Figure 4.1).
Spinal segmental instability occurs when the spine is unable to maintain its pattern of
displacement under physiologic load and is considered an important contributor to low
back pain (Mimura et al., 1994; Nachemson, 1985; Panjabi, 1992) and may involve
disease of the intervertebral disc (IVD) and the zygapophysial joints (ZJ), either singly
or in combination. The role of the ZJs in the lumbar spine is considered to be primarily
one of resistance to excessive rotary and shear forces (Farfan et al., 1972).
Figure 4.1: The lumbar functional spinal unit comprises the paired zygapophysial
joints, the intervertebral disc and the related muscles and ligaments (A); transverse
plane rotation occurs close to the posterior anulus ex vivo and anterior to the anulus in
vivo (B). Segmental rotation induces concurrent motion in the coronal and sagittal
planes (C).
Individual anatomical variation results in individualised movement patterns (Dupuis et
al., 1985). Most studies investigating axial rotation with human cadaveric material
report early structural failure at a mean range of over 2° per segment (Adams & Hutton,
1981; Ahmed et al., 1990; Farfan et al., 1970; Gunzburg et al., 1991; Liu et al., 1985;
Markolf, 1972; McFadden & Taylor, 1990; Schultz et al., 1979; Tencer et al., 1982).
During axial rotation the ZJ surfaces contralateral to the motion direction are
compressed while the ipsilateral joint surfaces separate from each other (Pearcy &
Tibrewal, 1984). These are termed ‘compression’ and ‘tension’ facets, respectively. The
axis of rotation migrates towards the compression facet as the range of axial rotation
increases (Wachowski et al., 2009). Additionally, axial rotation is normally coupled
with both coronal and sagittal plane rotations (Panjabi, 1992; Pearcy & Hindle, 1991).
The influence of ZJs is important in evaluation of any motion segment behaviour
A B C
Chapter 4: The Ex vivo CT study
Page IV-3
(Grobler et al., 1993). Coronally orientated joints confer less restraint to axial rotation,
(Cyron & Hutton, 1980; Farfan et al., 1972) with Duncan and Ahmed (Duncan &
Ahmed, 1991) noting more oblique orientation and flat geometry of the compression
facet facilitates axial rotation. An increase in axial rotation in the lumbar spine, when
moving from an extended to a flexed position, has also been observed (Duncan &
Ahmed, 1991). However, in vivo and cadaveric studies conducted by Gunzburg et al
contradict these findings; which in part reflects variations between ex vivo and in vivo
designs (Gunzburg et al., 1991). In subsequent investigations by Pearcy & Hindle of
ligamentous lumbar segments tested in the neutral position and then various ranges of
flexion, they confirmed that sub-maximal flexion increases the available axial torsion
range in the lumbar spine (Pearcy & Hindle, 1991).
Segmental instability has been considered an inevitable sequel to the degenerative
process, involving both the IVD and the ZJs, resulting in a temporary increase in motion
due to laxity of the connective tissue restraints (Haughton et al., 2002; Kirkaldy-Willis,
1988). A variable response to axial rotation in degenerated motion segments has been
observed in many studies (Adams & Hutton, 1981; Blankenbaker et al., 2006; Farfan et
al., 1970; Mimura et al., 1994). Segments with degenerated ZJs or IVDs have
demonstrated a larger neutral zone during rotation testing with aberrant motion patterns
at small ranges of rotation (Adams & Hutton, 1981; Farfan et al., 1970; Mimura et al.,
1994). According to Adams & Hutton, degenerated IVDs allow approximately 7° of
rotation per segment before failure, whereas normal segments confer <2° (Adams &
Hutton, 1981). End stage segment disease involving autofusion from osteophytosis is
intended to inhibit motion and finite element modelling confirms reduced axial rotation
range at intervertebral levels with higher grades of degeneration (Rohlmann et al.,
2006).
Visualisation of motion abnormalities in the lumbar segments has proven difficult,
(Pope et al., 1992; Reichmann, 1973) particularly with respect to axial rotation (Vrtovec
et al., 2010). With the advent of computed tomography (CT) and Magnetic Resonance
Imaging, anatomical assessment of the ZJs has improved, including an understanding of
their contribution to motion segment control. Zygapophysial joints have been implicated
in excess axial rotation motion in unstable cadaveric specimens (Yong-Hing et al.,
1976). In an attempt to demonstrate suspected clinical instability, Kirkaldy-Willis
Chapter 4: The Ex vivo CT study
Page IV-4
(Kirkaldy-Willis & Hill, 1979) recommended CT scanning in a supine rotated position
(the twist CT test). This demonstrated narrowing of the lateral recess and abnormal
separation in the tension facet (Kirkaldy-Willis & Tchang, 1988). The ‘twist CT’ has
been successfully employed in the cervical spine to examine rotation displacements in
normal and symptomatic populations (Dvorak et al., 1987; Penning & Wilmink, 1987).
Such a test was subsequently proposed by Graf (Graf, 1992) as a diagnostic predictor of
rotational instability in the lumbar spine. Graf considered separation of the lumbar ZJ
surfaces >1.5 mm as a diagnostic threshold for instability, however the basis for this
criteria has not been validated against normal reference ranges. Increased axial rotation
ranges using this test were demonstrated at degenerated segments in patients by
Blankenbaker et al which elicited concordant pain on subsequent discography
(Blankenbaker et al., 2006).
An important question has been to determine the normal and pathological response to
torsion. Using a low dose CT protocol to examine axial rotation in lower thoracic and
upper lumbar segments in normal male subjects, evident separation of the tension ZJs in
asymptomatic subjects was reported, although the actual rotation range per segment was
small (Singer et al., 1989). In a later study (Singer et al., 2001) using twist CT scans of
lower lumbar segments of 79 patients with lumbar spine disease significantly more
separation was shown in coronal compared with sagittal orientated ZJs.
Zygapophysial joint orientation and geometry, as well as degenerative changes,
potentially influence the response to lumbar torsion. The purpose of this study was to
examine the effect of torsion in cadaveric lumbar spine segments, by comparing axial
rotation with ZJ separation, then contrasting this response with macroscopic segment
degeneration of the mobile segments. It was anticipated that the anatomical morphology
of the ZJs coupled with the pathology of the motion segment would be associated with
the extent of separation under torsion load.
4.3 Methods
Thoracolumbar spine specimens obtained at autopsy were stored frozen at -20°C.
Anteroposterior and lateral radiographs were used to exclude any specimens with
evidence of prior surgery, tumour or ankylosis. The three cases of average height and
weight were designated A (male aged 61), B (male aged 85) and C (female aged 80
Chapter 4: The Ex vivo CT study
Page IV-5
years). Prior to testing, each case was thawed and cleaned of all muscle tissue leaving
the osteoligamentous spine intact from T12 to the sacrum.
The most superior and inferior vertebral bodies were positioned and fixed into cups
using titanium screws and bone cement, then secured in a custom torsion apparatus
(Figure 4.2A). Due to the lack of sacral fixation available in two cases (B&C), the L4-5
level was not tested in Case B and C. Once positioned into the torsion rig, each case was
orientated in neutral, or in 5° of flexion or extension.
The 3Space FastrakTM
(Polhemus, Vermont, USA) electromagnetic motion tracking
device was used to record the segmental movements in each case. Labview software
(National Instruments, USA) was used to control the Fastrak device and acquire motion
data.
Tracking sensors were attached to the lumbar vertebral bodies using rigid perspex
holders (Figure 4.2B). Case A was tested using torsional strain increments of 5, 10 and
15kg applied via pulleys using free weights. The lever arm of the rotation axis in the
torsion apparatus resulted in torsional loads of: 5Nm, 10Nm and 15Nm, respectively. To
accommodate creep each case was pre-loaded for 2 minutes prior to recording the range
of movement. In the older specimens (B and C), the 15kg load increment was not
applied to minimize risk of tissue failure. The range of right and left rotation was
measured under each load increment with the specimens in a neutral, then flexed
followed by extended positions. For this report only the 10Nm load data are presented.
Following motion measurement with the Fastrak system, each specimen was fitted into
the torsion apparatus, placed into a Perspex water tank, to simulate soft-tissues, and
scanned parallel with the superior vertebral end-plate of each candidate vertebra. A
lateral scout view in each unloaded position was obtained to facilitate alignment of the
CT gantry. The loading protocol used for the CT scanning was the same as for
recording Fastrak data.
Chapter 4: The Ex vivo CT study
Page IV-6
Figure 4.2: The torsion apparatus was positioned in situ within a water tank during
testing and scanning (A). To produce axial torsion in the specimen, load was
introduced by weights applied to cords around the proximal torque cup (TC). This cup
was restrained on the apparatus frame to provide fixation of the specimen into either:
neutral, 5° flexion or 5° extension. The Fastrak (F) tracking sensors (S) were attached
to Perspex stem holders which were screwed into the vertebral bodies of the specimen
(B).
The specimen was then removed from the torsion apparatus and segments dissected
transversely through the disc and posterior elements. Disc degeneration was graded
according to criteria described by Nachemson(Nachemson, 1960) (Grade I: normal,
Grade II: moderate degeneration, Grade III: advanced degeneration). The degenerative
status of the ZJs was macroscopically classified into four categories. Grade I: normal
A
B
Chapter 4: The Ex vivo CT study
Page IV-7
articular cartilage, Grade II: fine fibrillation, Grade III: coarse fibrillation, and Grade
IV: enurbation of articular cartilage to subchondral bone.
The CT images for every level were video-digitised, scaled and analysed using NIH
Image software (Image J, NIH Bethesda, USA,). For each image the paired ZJ angles
were derived from a median sagittal reference line (Figure 4.3A).
To calculate the separation of the ZJs, each joint was enlarged (x3) with bilinear
interpolation and a threshold established using the gray scale value of cortical bone. The
medial and lateral margins of the superior articular facets were marked to determine the
joint space length. From the mid point of this line, 2/3 of the joint space was divided
into regions. The separation of the joint for each region was measured and the average
separation of the articular surfaces defined (Figure 4.3B).
The image analysis process error was estimated by repeated measurements of one image
and calculating the coefficient of variation (CV). Using cortical bone to establish a
constant image threshold the intra-examiner CV was 1.6% for all measures.
Figure 4.3: From the CT image a sagittal median reference plane was established by
extending a line from the centroid of the vertebral body to the inter-laminar junction of
the posterior elements. A line drawn from the lateral to the medial borders of the
superior articular facet was extended to the medial sagittal reference plane and the
orientation of the zygapophysial joints, in degrees, was established (A). The CT scale
was used to reference the zoomed (x3) and thresholded image; then the midpoint of the
line determining the length of the joint, was used to calculate the physical separation of
the middle 2/3 of the joint space (B).
Chapter 4: The Ex vivo CT study
Page IV-8
Pilot studies using the Fastrak system indicated an accuracy of 0.01°, repeatability
coefficient of variation was 0.6%, and the system noise in the laboratory was 0.01°.
Descriptive statistics were used to present trends for rotation responses. The association
between the zygapophysial morphology and separation was assessed with simple linear
regression. A probability of p<0.05 was used as the criterion to reflect a meaningful
association.
4.4 Results
The results for each case are presented in four sections describing I: the ZJ orientation
and degenerative grade of the motion segments, II: the axial-torque response, III: the ZJ
separation in response to torsion and, IV: the influence of sagittal position on axial
rotation and ZJ separation response.
I: Zygapophysial joint orientation and degenerative grading of mobile segments
Case A demonstrated a gradual caudal increase in coronal ZJ alignment, Case B showed
predominantly sagittal orientation, and Case C presented more coronal orientatation.
The ZJ surfaces differed geometrically between cases. Case A had relatively flat joint
surfaces by comparison, Case B demonstrated ‘J’ shaped joints with large restraining
mammillary processes, while Case C demonstrated deep ‘C’ shaped joints. Relative ZJ
symmetry was present at all levels, however as variations of less than 6° are considered
normal, only three segments fulfilled the criteria for asymmetry (Table 4.1).
Figure 4.4 illustrates the macroscopic CT features at the level of the superior end-plate
for each case at the L3-4 level, contrasting: neutral, left and right torsion responses
under a 10Nm load.
Table 4.1: Segmental orientation of the zygapophysial joints as measured from the sagittal
reference plane. Orientation of the right and left joints for each case are reported (data are
in degrees).
Case A Case B Case C
R L R L R L
L1-2 13.6 15.7 7.2 11.1 36.6 33.0
L2-3 31.9 36.8 17.6 11.1 * 31.1 42.6 *
L3-4 37.9 38.9 25.7 30.4 45.8 37.2 *
L4-5 49.1 54.3 – –
(*: denotes zygapophysial joint asymmetry > 6)
Chapter 4: The Ex vivo CT study
Page IV-9
Figure 4.4: The rotation sequences for all cases at level L3/4 are presented. The CT
sections were obtained after 10Nm load to the right (I) and to the left (II). The middle
image (N) in all cases represents no load. Note the different anatomical and geometrical
configurations of the posterior joints. The flat joint surfaces of Case A, compared to the
sagittally aligned joints in Case B. In Case C, the ‘C’ shaped geometry of the
zygapophysial joints can be observed, in particular, the excessive separation following
rotation.
Chapter 4: The Ex vivo CT study
Page IV-10
The degenerative condition of the ZJs were similar. Apart from three upper lumbar
segments, other levels showed marked fibrillation or enurbation of the articular
cartilage. In general, the articular cartilage of the sagittal component of the joints
demonstrated greater change than the coronal component. Posterior margin osteophytes
were noted on the right side of the ZJ at L3-4 in Case B. The degree of IVD
degeneration was similar for Cases A and B. Large osteophytes were noted laterally on
the right side of the L3-4 in Case A, while at L1-2 in Case B there was calcification in
the outer anulus with anterior osteophytes. All IVD’s for Case C demonstrated marked
degeneration with calcification of the outer anulus. Macroscopic degenerative
classification of the ZJs and IVDs for all motion segments is presented in Table 4.2.
Table 4.2: Macroscopic degenerative changes of the zygapophysial joints and
intervertebral discs.
Case A Case B Case C
Joint
Degen
Disc
Degen
Joint
Degen
Disc
Degen
Joint
Degen
Disc
Degen
R L R L R L
L1-2 II I III III II III II III III L2-3 IV III III IV III III IV III III L3-4 IV III III III IV III IV IV III L4-5 IV IV III
II: Axial torque response
Axial torque data were recorded for each specimen by using the cranial vertebra of each
motion segment as a reference point and subtracting the angle of each subjacent level
(Table 4.3). The mean segmental unilateral axial rotation response for Case A, under 10
Nm, was 1.2° (range 0.28° - 2.66°). For Case B a mean of 2.6° (range 0° - 3.02°). Case
C demonstrated the highest mean of 3.7° (range 1.94 - 5.28°). Segmental rotation angles
were generally greater in the lower than the upper lumbar spines. An example of the
axial torque-rotation response, for the L3-4 segment of each case, under 10Nm load for:
neutral, flexion and extension positions, is presented in Figure 4.5.
Chapter 4: The Ex vivo CT study
Page IV-11
Figure 4.5: Graphical presentation of the right and left rotation response in each case at
L3/4 under 10Nm loading.
Table 4.3: Summary of axial plane motion for all cases, in a neutral position. Rotation in
the axial plane was derived from Fastrak and was measured after 10 Nm loading of the
specimens. (Data are in degrees).
Case A Case B Case C
R L R L R L
L1-2 0.36 0.28 0.01 2.21 1.94 2.89
L2-3 0.52 0.54 2.83 3.02 3.58 3.54
L3-4 1.82 2.66 2.98 1.92 5.28 5.22
L4-5 2.20 1.25 – –
III: Imaging of zygapophysial joint separation in response to torsion
Following rotation loading the ZJ space ipsilateral to the movement direction widened.
Under 10Nm loading in the neutral position, the mean joint separation for Cases A & B
was 2.3mm (range 1.8 - 2.9mm) and 2.3mm (range 1.3 - 3.0 mm), respectively. In
contrast the mean separation in Case C was more marked at 3.8mm (range 2.9 -
5.1mm). The left to right separation response, for each level following 10Nm load in the
neutral position, is presented in Table 4.4.
The measured separation was greater for the lower lumbar segments in Cases A and C.
The separation in Case B was similar for all levels except L2-3 where it increased
following right rotation and decreased at L3-4 following left rotation. The ZJ separation
Chapter 4: The Ex vivo CT study
Page IV-12
response to 10Nm load of the L3-4 segment in each case is depicted in Figure 4.6
revealed a significant correlation (R2 0.69, p<0.001).
To appreciate the separation response in relation to the torque-rotation loading
increments, all cases were scanned in semi-flexed and extended positions. The ZJ
separation in the tension facets, demonstrated that the majority of the separation
occurred under minimal loading, in neutral, semi-flexion and extension.
Table 4.4: Summary of tension zygapophysial joint separation in millimeters for all
Cases, in a neutral position with 10Nm loading.
Case A Case B Case C
R L R L R L
L1-L2 1.80 2.16 2.39 2.46 2.96 3.81
L2-L3 2.28 1.88 3.00 2.42 3.58 3.60
L3-L4 2.55 2.79 2.22 1.37 3.50 5.06
L4-L5 2.50 2.86 – –
Figure 4.6: The association between the separation response at levels for all cases.
Each case was clustered according to the relative degree of degeneration exhibited, with
Case C showing the widest separation and segmental rotation as a function of the stage
of age-related changes.
Chapter 4: The Ex vivo CT study
Page IV-13
IV: Effect of sagittal position on axial rotation and zygapophysial joint separation
response
Segmental flexion achieved slightly more rotation compared with neutral under the
10Nm load (Table 4.5), with a trend to a reduction in mild extension. Similar trends
were observed for ZJ separations of the tension facet which increased in semi-flexion,
and decreased or no change in the semi-extended position.
Table 4.5: Combined left and right segmental rotation responses for L1-2 to L4-5,
recorded by Fastrak 3D system for three cases subjected to a 10Nm torsional
strain.
Case A Case B Case C
Neutral
L1-2 0.6 2.2 4.8
L2-3 1.1 5.8 7.1
L3-4 4.5 4.9 10.5
L4-5 3.5 – –
5 ° Flexion
L1-2 0.7 2.1 6.8
L2-3 1.5 5.5 6.5
L3-4 4.6 3.7 7.3
L4-5 2.6 – –
5° Extension
L1-2 0.6 1.4 3.8
L2-3 1.0 5.0 7.5
L3-4 3.2 4.2 9.5
L4-5 2.3 – –
All data are degrees (°)
4.5 Discussion
This study examined the response to incremental axial rotation loading in three
cadaveric lumbar spines, each representing stages in age-related spine disease of the
IVD and ZJ of their respective motion segments.
As expected, the torsion responses and zygapophysial separation between and within
cases, reflected individual variations in joint morphology and phase of degeneration of
the mobile segment. The ranges of segmental rotation recorded were similar to those
previously reported (Ahmed et al., 1990; Farfan et al., 1970; Gunzburg et al., 1991).
There was a general trend towards increased axial rotation in the more coronally
oriented lower joints (Table 4.3). The more advanced degeneration in Cases B and C
Chapter 4: The Ex vivo CT study
Page IV-14
may explain their increased rotation range relative to Case A. The IVDs of these
specimens all showed advanced degeneration which may have contributed to an
increased range of axial rotation. In these three cases, asymmetry of the paired
zygapohysial joints was not marked and did not appear to influence the rotation.
The effects of change in sagittal plane posture on the axial rotation response measured
in the current study support the findings of Pearcy and Hindle (Pearcy & Hindle, 1991).
Segments semi-flexed up to 5° generally showed a slight increase in axial rotation range
compared to the neutral position. This decreased range in full flexion acts to ‘unlock’
the ZJs but putatively increases shear compression of the anteromedial region of the ZJs
and increases tension in the posterolateral anulus. The 5° extension achieved in all cases
resulted in an overall reduction in rotation in all segments, or was equivalent to ranges
produced in the neutral position. This finding is explained by the greater approximation
of the ZJs into extension positions.
There are numerous descriptions in the literature of lumbar ZJ separation in response to
axial rotation. The tension facet was reported by Farfan et al (Farfan et al., 1970) in
some cases to open by 10mm before failure. Liu et al (Liu et al., 1985) measured a
cartilage filled gap of about 1.5mm between ZJ surfaces and suggested the articular
cartilage may be compressed 60% during rotation. Separation in the tension facet is a
normal ZJ response rather than a sequel to injury or part of segmental instability. The
separation response is not only explained by orientation of the joints alone, as their
shape, integrity of the ligamentous capsule and IVD, also influence this response. In
Case C the marked enurbation of articular cartilage contributed to the greater separation
of the tension facets compared to Case A.
All specimens tested demonstrated moderate to advanced degenerative changes to their
functional spinal segments. The condition of the ZJ cartilage was similar for most cases
with Case C also exhibiting the most degenerated discs which may have contributed
more ‘free play’ before firm apposition occurred in the compression facet (Adams &
Hutton, 1981). Greater laxity was noted by Farfan et al (Farfan et al., 1970) during
torsion in segments with degenerated discs and consequently their torque-rotation
curves were initially flatter. Similarly Mimura et al (Mimura et al., 1994) found an
increase in the neutral zone of the axial rotation range in segments with disc
degeneration. The instantaneous axis of rotation (IAR) in degenerated motion segments,
has been demonstrated to lie in the posterior part of the IVD (Farfan, 1973). As the IAR
Chapter 4: The Ex vivo CT study
Page IV-15
moves from the vicinity of the ZJ into the disc, more of the rotation constraint is
demanded of the ZJs (Haher et al., 1992). The recent in vivo study by Xia et al (Xia et
al., 2010) of lumbar segment response to transverse plane motion highlighted a marked
discord in IAR position between ex vivo investigations and in vivo studies. In part these
differences are assumed to be due to imposed constraints of the torsion rig compared
with true physiological rotation axes.
The separation response observed in the current case series may be explained by the
advanced IVD degeneration in the material tested along with the sustained nature of the
load regime during the CT sequences.
In Case A, the CT scans were taken under three increments of loading and the
separation measured. Interestingly most of the separation response was detected after
the first increment of loading (5Nm), the subsequent two increments adding little to the
response. This may suggest that the separation of the facets is first a response to
compression of the articular cartilage and secondly a function of the altered neutral
zone.
Axial rotation is normally constrained in the lumbar spine by the anulus of the IVD and
the lateral aspect of the zygapopysial joints, reflected in the typically limited range of
physiological rotation. A limitation of the instrument used to induce torsion in these
cases was the constrained nature of end-fixation which did not allow physiological
coupled motion of an unrestrained spinal segment.
These cases highlight the variable behaviour of the ZJs under axial rotation loads. To
fully understand the ZJ separation response, more elaborate torsion systems are required
utilizing unconstrained tissues which enable more physiological motion patterns to
occur. As zygapophysial separation is influenced by both anatomical and pathological
factors, an improved understanding of their contributions may be gained from studies
examining the torsion response in tissues which reflect the normal through to advanced
stage pathology continuum. Imaging of the response of the IVD, particularly the
nucleus pulposus, to rotation may elucidate the mechanics of this structure and its
response to segmental rotation.
Chapter 4: The Ex vivo CT study
Page IV-16
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226-34.
CHAPTER 5
Page V-1
The normative cohort MRI study
5.1 Summary
Rotation is frequently implicated as a mechanism by which the anulus fibrosus of the
intervertebral disc (IVD) is injured resulting in herniation of the nucleus pulposus (NP).
There are few data reporting the in vivo mechanical deformation of the NP in response
to sustained rotation. Rotation is coupled with lateral flexion as a composite movement.
Magnetic resonance imaging (MRI) provides a non invasive method of examining NP
deformation by mapping the hydration signal distribution within the IVD.
T1 weighted coronal and sagittal lumbar images and T2 weighted axial images at
L1-2 and L4-5 were obtained from 10 asymptomatic subjects (mean age 29, range: 24 –
34years) in sustained flexed, extended positions plus combined positions of left rotation
with flexion and extension. NP deformation was tracked by mapping the mean change
in hydration profiles from coronal and sagittal pixel measurements. Pooled data were
compared between positions.
An average sagittal change in range of 44° (SD 14.5°) from flexion to extension was
recorded between L1 and S1 (range: 18° – 60°) which resulted in a mean anterior NP
deformation of 16 % of disc hydration profile (range: 3.5% – 19%). On average a 4.8%
coronal deformation of nucleus was recorded when rotation was coupled with either
flexion or extension (SD – 5.1%; range: 0.4% – 15%). Lateral nucleus deformation
direction was variable with respect to left rotation (44% deformed to the left and 56%
deformed to the right). The direction of intersegmental lateral flexion had a more
consistent influence on NP deformation direction with 75% of NPs deforming to the
contralateral side.
Direction of NP deformation following lumbar sagittal plane positional change was
predictable with 19/20 cases deforming towards the opposite direction. Deformation of
the NP following adoption of rotated positions in flexion and extension was reduced in
magnitude and less predictable with respect to direction. In 75% of cases the NP
deformed contralateral to the direction of intersegmental lateral flexion.
Chapter 5: The normative cohort MRI study
Page V-2
5.2 Introduction
The intervertebral disc (IVD) is a primary load bearing structure in the lumbar spine,
designed to attenuate compressive force using hydrostatic properties afforded by the
high proteoglycan content of the nucleus pulposus (NP). Offset compressive load will
typically result in deformation towards the area of least compression. The boundary of
the NP is constrained by an intact anulus. However, anular compromise combined with
compressive load may result in symptomatic disc bulge, protrusion or herniation.
Rotation movements are often implicated as an injuring mechanism for the IVD
(O'Sullivan, 2005) especially when performed under load and in a preloaded flexed
position. There is limited ex vivo evidence for the mechanical effect of axial rotation on
the anulus fibrosus (AF) and zygapophysial joints (Adams et al., 1981b; Farfan, 1984;
Farfan et al., 1970) and less again for the in vivo effects on nucleus pulposus
deformation (Fazey et al., 2006).
Lateral flexion and axial rotation are not independent during spinal motion (Cholewicki
et al., 1996; Lovett, 1905.) This biomechanical coupling occurs when primary motion in
either a coronal or axial plane induces secondary motion in the other (White et al.,
1990).
The direction of coupled lumbar segmental motion is controversial and presumed to be
relative to sagittal plane spinal position (Cholewicki et al., 1996; Pearcy et al., 1984a;
Russell et al., 1993). The literature reports coupling patterns are variable in direction
and between intervertebral levels (Panjabi, 1989; Pearcy et al., 1984b; Plamondon,
1988; Vicenzino et al., 1993). Examination of spinal rotation effects must therefore also
include the influence of associated coronal plane motion.
The anatomy of the lumbar spine limits axial rotation to approximately 2°
intersegmentally (Singer et al., 2004). Passive restraint to axial rotation is conferred by
the zygapophysial joints, their ligaments and the intervertebral discs (Adams et al.,
2002). Collagenous fibres of the anulus constrain interbody rotation. Krismer (1996)
reported that selective sectioning of unidirectionally oriented anular fibres resulted in a
2° increase in axial rotation range while bilateral facetectomy resulted in a 1.2° increase
in range. On this basis the anulus was hypothesized to be the primary restraint to
rotation. Others have ascribed control of rotation range to the zygapophysial joints
(Adams et al., 1981a; Shirazi-Adl, 1991; 1994). Torsional stiffness is increased under
Chapter 5: The normative cohort MRI study
Page V-3
compressive load (Goodwin et al., 1994) and conversely loss of torsional stiffness
correlates with increased severity of rim lesions in the IVD (Thompson et al., 2000).
Haughton et al (2002) reported a correlation between increased ranges of intersegmental
lumbar rotation in degenerate discs and discogenic pain (Haughton et al., 2002).
Rotation range varies between the upper lumbar segments with sagittally oriented facets
to the lower lumbar segments where facets typically exhibit more coronal orientation
and greater rotation range (Singer et al., 2001).
Segmental rotation range varies with the degree of sagittal plane positioning. Greater
ranges are seen in sub maximal flexion as the facets disengage and are less able to
constrain rotation. Smaller ranges are reported in maximal flexion as ligamentous
structures tighten and forward translation shear engages the articular facets against those
of the subjacent level (Pearcy et al., 1991).
In vivo studies of segmental rotation are technically difficult. Steinman pins inserted
into spinous processes have been used to measure motion (Gregersen et al., 1967;
Gunzberg et al., 1991) however, such invasive methods potentially influence results.
Magnetic resonance imaging provides an elegant, non invasive choice of imaging from
which to measure in vivo deformation of the NP.
Previous studies have used MRI to examine the effect of sagittal plane positioning on
NP movement (Alexander et al., 2007; Beattie et al., 1994; Brault et al., 1997;
Edmondston et al., 2000; Fennell et al., 1996). Different methods were used to track NP
deformation including visual inspection and measurement of the displacement of the
point of maximum pixel intensity relative to changes in subject position.
Axial MR image analysis has demonstrated increased ranges of intersegmental rotation
in normal and degenerate discs (Haughton et al., 2002).
Fazey et al (2006) confirmed a reliable MRI based method to quantify the mean NP
deformation which occurred in response to sagittal position change and rotated positions
of the lumbar spine.
The aim of the present study was to test the consistency with which left rotated postures
influenced NP deformation in positions of flexion and extension at L1-2 and L4-5 using
T2 weighted magnetic resonance imaging. It was hypothesized that in a relatively young
Chapter 5: The normative cohort MRI study
Page V-4
normal cohort that the NP would deform in a predictable way relative to sagittal, axial
and conjunct coronal plane segmental positions.
5.3 Methods
Ten asymptomatic subjects, five male and five female with a mean age of 29 years
(range: 24 – 34 years) were recruited to the study. Inclusion criteria sought subjects with
no significant previous history of back pain requiring intervention within the preceding
year, and a body size and shape amenable to positioning within the confines of the MRI.
Subjects were excluded by the presence of any contraindications to MRI including
claustrophobia and the presence of ferrous implants. Institutional Ethics approval was
obtained and all participants provided written informed consent.
Each subject was initially positioned supine on the gantry of 1.5T MR imager (Siemens,
Berlin, Germany). A cylindrical roll of towel was placed under the lordosis to
accentuate extension of the lumbar spine (Figure 5.1A). T1 weighted localizer sagittal
and coronal images (TR/TE [24/6], field of view 400mm, 512x512 matrix) and T2
weighted axial images (TR/TE [5160/102], field of view 210mm, 384x384 matrix) were
acquired with a fast spin echo sequence at the candidate levels L1-2 and L4-5. The
subject was then positioned into left rotation, while maintaining the extended position,
by the addition of a dense foam wedge cushion under the left hemipelvis and image
sequences repeated.
Lumbar spine flexion positioning (Figure 5.1B) prior to image acquisition was achieved
by placement of wedge cushioning under the sacrum and thorax with pillows to support
the flexed cervical spine and knees. Left trunk rotation was induced by the addition of a
wedge cushion under the left hemipelvis in the flexed position.
Intersegmental lateral flexion direction and range was measured on coronal images as
the angle formed by lines extended from superior and inferior end-plates of adjacent
target levels L1-2 and L4-5.
Chapter 5: The normative cohort MRI study
Page V-5
Figure 5.1: Subject positioning on the gantry of the MRI. Cylindrical bolster (arrow)
under lumbar spine to induce extension (A) and wedge cushioning under thorax and
sacrum (not visible) to induce flexion (B). (Image used with permission from Clinical
Biomechanics)
Cobb angles were derived from magnified sagittal images from the superior end-plates
of L1 and S1 to measure range of sagittal plane positional change from flexion to
extension (Figure 5.2).
Figure 5.2: Cobb angles (θ) were derived from sagittal images to measure change in
position from extension (A) to flexion (B).
A
B
A B
Chapter 5: The normative cohort MRI study
Page V-6
Mid disc axial images for all positions, assumed to optimally represent relative IVD
hydration, were selected for pixel profile analysis (Fazey et al., 2006) (Figure 5.3).
Using imaging software (NIH Image-J, Bethesda, USA) pixel intensity measurements in
sagittal and coronal planes were derived by placing three lines through the mid disc area
from anterior to posterior anulus and from right to left respectively. Raw data were
normalized to 100 points and then averaged within a Labview software routine
(National Instruments, Austin, USA) (Figure 5.3). Averaged line data were then
expressed as a percentage of the whole for each half of the line.
Figure 5.3: Axial images showing orientation and position of 3 lines in coronal and
sagittal planes from which pixel data were derived (A). Raw pixel data for each line
graphed against 100 point scale.
Inter and intra rater reliability was assessed by coefficient of variation (CV) from
repeated measures of Cobb, lateral flexion angles and pixel intensity.
5.4 Results
Acceptable intra rater reliability was demonstrated from repeated measures of all
dependent variables with CV of 3% for Cobb angle and 3.1% and 2.8% for lateral
flexion angles and pixel intensity measurements, respectively.
Obliteration of the contralateral zygapophysial joint space was seen at all levels and
segmental rotation was noted to have occurred in all cases.
The mean difference in position from flexion to extension between L1 and S1, was 44°
(SD 14.5°; range: 18° – 60°), mean lateral flexion range at target levels was 3.4° (SD –
1.85°; range: 0° – 7°).
A B
Chapter 5: The normative cohort MRI study
Page V-7
With a change of sagittal plane position from flexion to extension, 19/20 discs
demonstrated a mean anterior NP deformation of 16% (range 3.5% – 19%). One disc
(L4-5) demonstrated a reverse directional trend (8.6%) following moving from an
extended to a flexed position.
The mean coronal offset of NP in the left rotated position was 4.8% of pixel profile
(SD 5.1%; range 0.4% – 15%) irrespective of sagittal plane position with 9 of 20 discs
demonstrating an increased NP offset to the left, and 11 of 20 to the right (Table 5.1).
Mean coronal NP deformation in extension derived from pooled data for both
intervertebral levels was 3.7%. While in flexion this was comparatively greater (mean –
5.9%), the difference was not significant p = 0.08 (Figure 5.4).
Figure 5.4: A trend towards mean coronal NP bias reduction in the extended and left
rotated position was evident at both intervertebral levels though not statistically
significant.
The direction of intersegmental lateral flexion relative to direction of NP bias was
contralateral in 15 discs and ipsilateral in 5 discs (Table 5.1).
Chapter 5: The normative cohort MRI study
Page V-8
Table 5.1: Direction and magnitude of NP migration relative to position.
Lumbar Spine Position NP migration direction (n) NP shift (range)
Extension Anterior (19/20) 16% (3.5-19)
Posterior (1/20)
Left Rotation +
Flexion/extension
Left (9/20)
Right (11/20)
5.5% (0.4-15)
5.5 Discussion
The hypothesis that the NP would deform away from the area of primary compression
of the IVD was sustained for sagittal plane supine postures but was more variable in
rotation related to the direction of the associated lateral flexion more than rotation.
Ranges of sagittal plane position change from extension to flexion were comparable to
previous MRI studies though somewhat less than those performed in open magnets.
This difference reflects the spatial constraints within the bore of a conventional magnet.
Axial intersegmental range was assumed to be maximal by obliteration of
zygapophysial joint space on the contralateral side and widening ipsilaterally.
Intersegmental lateral flexion was a secondary coupled response to the primary position
of rotation and therefore not expected to demonstrate full available range.
In the lumbar spine each degree of segmental axial rotation is accompanied by two
degrees of lateral flexion (Cholewicki et al., 1996) therefore it is not unexpected that the
lateral flexion component of the composite position would have the greater effect on NP
deformation.
Hydrated discs behave as a hydrostatic mechanism and as such will deform towards an
area of least load. Compressive force being greater on the side of concavity, the
expectation is for deformation of the NP towards the convexity (Périé et al., 2001;
Violas et al., 2005).
This study, however, revealed that 75% of NPs examined deformed towards the coronal
plane convexity in the rotated position and 19/20 (95%) towards the sagittal plane
convexity in the extended position. Some previous studies have reported similar NP
behaviour in response to sagittal plane position and suggested that predictability may be
reduced in the presence of degenerative change (Edmondston et al., 2000; Schnebel et
al., 1988). In the current study, the single NP that deformed posteriorly in extension did
not exhibit visual features of degenerative change. It may be speculated that greater
tensile force generated in the capsular portion of the anterior anulus than that of the
Chapter 5: The normative cohort MRI study
Page V-9
compressive force posteriorly will result in deformation towards the area of
compressive load. Further study comparing tensile and compressive forces within the
IVD would be required to test this hypothesis.
Reduced NP deformation magnitude reported at both intervertebral levels in extension
plus left rotation may reflect reduced range of available segmental axial rotation in
extended positions (Haberl, 2004). Additionally, increased range of lumbar segmental
axial rotation has been demonstrated in submaximal flexion (Pearcy et al., 1991) and
may contribute to observed differences.
The variable NP deformation in left rotated postures may relate to the scanning
methodology.
Previous studies profiled peak pixel points from a single line through the mid disc,
assuming these to represent the centre of the NP and therefore a consistent point for
inter-individual comparison (Alexander et al., 2007; Edmondston et al., 2000).
Observation of graphed pixel intensity frequently reveals numerous points of higher
pixel intensity representing relative hydration, even when data from three lines were
averaged. A methodology such as that employed in the current study that calculates
strength of hydration signal offset from multiple samples rather than a single point, may
therefore be more representative of NP deformation patterns.
Although speculative, results of this preliminary normative study may have implications
for the contribution of rotation and lateral flexion to lumbar disc injury and patterns of
disc herniation. Axial rotated positions in supine appear to have a less predictable effect
on NP deformation, than lateral flexion. It may therefore be of interest to determine the
relationship between injuring mechanisms and herniation patterns in symptomatic
individuals.
Study limitations include the confines of the MR constraining sagittal range of motion
to sub maximal. Segemental lateral flexion, as a secondary response to primary rotation,
was unlikely to be to the maximum available range. Disc sampling for hydration
profiling was limited to two dimensions; three dimensional imaging would enable a
composite analysis of the entire target disc. Imaging was commenced with subject pre
positioning in the sagittal plane. Data derived from this position was compared with that
of the subsequent combined positioning. Imaging and analysis of NP hydration
weighting in the resting neutral position would provide greater insight into the
Chapter 5: The normative cohort MRI study
Page V-10
comparative deformation by excluding any effect of pre positioning on the IVD. Data
derived from coronal images for lateral flexion direction and magnitude may be
influenced by slice orientation. A slice angle posterior to the axis of motion may
partially reflect sagittal plane position. The likelihood of this is increased with regional
rotation. Future investigations should employ coronal images adjusted to each scanned
level.
A future study would be recommended to test the effect of primary coronal plane
positioning into lateral flexion to more accurately determine comparative predictability
of NP deformation direction between coronal and axial plane postures.
5.6 Conclusions
This study has shown that in young asymptomatic individuals the NP at L1-2 and L4-5
deforms predictably away from offset compressive load in positions of flexion and
extension. The direction of NP deformation following left rotation in flexion and
extension is unpredictable. Deformation relative to the direction of secondary
intersegmental lateral flexion is more predictable as 75% of cases deformed away from
the direction of lateral flexion.
Chapter 5: The normative cohort MRI study
Page V-11
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1990;
CHAPTER 6
Page VI-1
The lateral flexion cohort MRI study
6.1 Summary
While there are numerous studies examining aspects of sagittal plane motion in the
lumbar spine, few consider coronal plane range of motion and there are no in vivo
reports of the response of nucleus pulposus (NP) displacement in lateral flexion. This
study quantified in vivo NP deformation in response to side flexion in healthy
volunteers. Concomitant lateral flexion and axial rotation range were also examined to
evaluate the direction and extent of NP deformation.
Axial T2 and coronal T1 weighted Magnetic Resonance Images (MRI) were obtained
from 21 subjects (mean age: 24.8 years) from L1 to S1 in the neutral and left laterally
flexed position. Images were evaluated for intersegmental ranges of lateral flexion and
axial rotation. A novel method derived linear pixel samples across the width of the disc
from T2 images, from which the magnitude and direction of displacement of the NP
was determined. This profiling technique represented the relative hydration pattern
within the disc.
The NP was displaced away from the direction of lateral flexion in 95/105 discs
(p<0.001). The extent of NP displacement was associated strongly with lateral flexion at
L2-3 (p<0.01). The greatest range of lateral flexion occurred at L2-3, L3-4 and L4-5.
Small intersegmental ranges of axial rotation occurred at all levels but were not
associated with NP displacement.
The direction of NP deformation was highly predictable in laterally flexed healthy
lumbar spines; however, the magnitude of displacement was not consistent with the
degree of intersegmental lateral flexion or rotation.
Chapter 6: The lateral flexion cohort study
Page VI-2
6.2 Introduction
An increased knowledge of lumbar spine pathomechanics has improved our
understanding of the cause and effect of low back pain. However, a major focus has
been on sagittal plane motion, particularly flexion, on the assumption that this
represents the most functional lumbar motion (Adams et al., 2002). Sagittal motion also
contributes the greatest directional range and is most often implicated as an injuring
mechanism (Pearcy et al., 1984a). Axial and coronal plane motions, however, are
important components of spinal segmental mobility but have not attracted the same
attention in the literature due to the complexities of coupled motion.
Existing literature focuses on regional range of coronal plane motion (Kachingwe et al.,
2005; Schuit et al., 1997) and on functional consequences related to sports (Burnett et
al., 1998). Earlier studies on intersegmental range (Dvorak et al., 1991; Pearcy et al.,
1984b) provide limited insight into the mechanics of lateral flexion. Little consideration
is given to the effect of lateral flexion on the intervertebral disc (IVD). As IVD
dimensions in the coronal plane are approximately 50% greater than in the sagittal plane
it is reasonable to infer that lateral movement will generate higher stress distributions
within the IVD than sagittal displacement (Adams et al., 2002). Combinations of
movement in both planes can generate very high intradiscal and anular tensile strains
especially when combined with axial rotation (Steffen et al., 1998) and as such are
implicated in injury (Adams et al., 2002; Scannell et al., 2009).
Lateral flexion and axial rotation are coupled movements within the lumbar spine
(White et al., 1990). It is well known that primary movement in one plane induces
movement in the other, likely through the combined influence of bony architecture,
intervertebral disc, ligamentous compliance and muscle action (Scholten et al., 1985).
However dispute exists over the relationships between axial and coronal plane
contributions (Legaspi et al., 2007). Despite this, assessment of motion in one direction
should give due consideration to the other.
The nucleus pulposus (NP) by virtue of high proteoglycan content, acts hydrostatically
to attenuate load through the disc and distribute force to the anulus and end plates.
Examination of hydration profiles within the NP can therefore reflect deformation
patterns in response to offset loading. Several in vivo studies of healthy individuals,
employing Magnetic Resonance Imaging (MRI), have reported IVD deformation in the
sagittal and axial plane (Brault et al., 1997; Edmondston et al., 2000; Fazey et al., 2006;
Chapter 6: The lateral flexion cohort study
Page VI-3
Fennell et al., 1996) and in scoliosis (Périé et al., 2001). Limited data on NP
deformation in lateral flexion exist mainly from cadaver studies (Tsantrizos et al.,
2005); however, no investigations to date have reported in vivo NP deformation in
response to induced lateral flexion.
MRI provides an elegant method of examining NP response to postural changes of the
spine. Novel methods of image analysis using T2 weighted MRI images have
previously been used to quantify NP deformation (Fazey et al., 2006). This hypothesis
generating study sought to quantify in vivo NP deformation in response to side bending
in healthy volunteers. Additionally, the association between lateral flexion and axial
rotation range were examined to evaluate the direction and extent of NP deformation.
6.3 Methods
A total of 21 healthy volunteers were recruited to the study; 11 female and 10 male,
with a mean age of 24.8 years (range: 20-34). Exclusion criteria included
contraindications to MRI or significant degenerative disc disease as assessed by two
orthopaedic surgeons (Y.I & Y.S.). Prior to the study, institutional ethics approval was
obtained and each subject provided written consent.
Subjects were initially positioned supine on the gantry of a 0.2T horizontally open MRI
unit (AIRIS mate, Hitachi Inc., Sopporo, Japan). The gantry was inserted into the
magnet and a series of T1 and T2 weighted images acquired first in the supine neutral
position then, following re-positioning, sequences were repeated in the laterally flexed
posture.
The axial T2 relaxation sequences were acquired through the mid disc region from L1-2
to L5-S1 with a fast spin echo sequence (3120/120 (TR/TE), FOV 260), 8mm slice
thickness and an acquisition time of 6:52 min. Slice position was manually determined
from planning images and the slice thickness was optimised at each segment to sample
the disc volume.
The pelvis was then stabilised with a strap to prevent rotation and the subject was
positioned into left side bending with one assistant manually holding the knees to
prevent lateral movement. The subjects were then asked to actively laterally flex to the
limit of their range. A second assistant applied overpressure at the shoulders to
minimise trunk rotation and to achieve a limit of lateral flexion range, which was
Chapter 6: The lateral flexion cohort study
Page VI-4
maintained passively by the assistants during imaging. Mid disc image sequences at all
levels were repeated using the same parameters.
To evaluate segmental rotation, axial T1 weighted images were taken through the bony
vertebra of L1 to S1 using a fast spin echo sequence (385/24.5 (TR/TE), FOV 300) slice
thickness 6mm, acquisition time 5:45 min. Finally coronal T1 images (285/24.5
(TR/TE), FOV 300; 6mm thickness, 1:34 min), which were optimal for demonstration
of the bony anatomy, were used to examine lateral flexion (Figure 6.1).
Figure 6.1: Coronal T1 weighted image demonstrating lumbar spine lateral flexion
achieved by subject positioning.
6.3.1 Image analysis
From the T1 axial images, rotation angles were calculated by a line from the spinous
process of each vertebra to the midpoint of the vertebral body. The vertical image frame
was referenced as the sagittal plane and the angle subtended between each was recorded
as the degree of axial rotation of that segment. For the S1 segment a line taken from the
sacral promontory to the mid point of the S1 body was extended posteriorly (Figure
6.2A).
Chapter 6: The lateral flexion cohort study
Page VI-5
Figure 6.2: Calculation of lumbar segment rotation angles from axial images (A) and
modification of the Cobb method for calculating segmental lateral flexion angles (B).
Lateral flexion intersegmental angles were calculated from the T1 weighted coronal
images. Using image analysis software (NIH Image-J, Bethesda, USA), the corners of
each vertebral body from L1 to L5 were identified and marked. The angle was then
measured at the intersection of the lines extending through the midpoints between the
two anterior and two posterior corners (Figure 6.2B). Derived angles were measured
twice by two blinded assessors resulting in high reliability (ICC 0.99).
Direction of NP deformation was derived from the neutral and laterally flexed T2
weighted mid-disc axial images using a previously described technique (Fazey et al.,
2006) and image analysis software (NIH Image-J, Bethesda, USA). This technique
enabled pixel intensity profiling to represent the relative hydration pattern within the
disc.
On neutral and laterally flexed axial images at each intervertebral level from L1-2 to
L5-S1, three lines were placed across the mid-disc region from right to left (Figure 6.3).
Raw pixel data from these line samples were normalised to 100 points, averaged using a
Labview software routine (National Instruments, Austin, USA), then imported into
Excel where the direction, extent and pattern of hydration was derived for neutral and
laterally flexed image pairs.
Chapter 6: The lateral flexion cohort study
Page VI-6
The NP did not consistently show a symmetrical profile in the neutral position.
Inevitably there was a small directional offset of the NP to either side. This variable was
taken into account in the calculations for NP deformation direction and extent.
Figure 6.3: Measurement of pixel intensity in neutral and laterally flexed positions.
Averaged pixel data were sampled from three coronal lines per segment from the paired
T-2 weighted axial images to represent the relative hydration pattern of the NP. Trunk
rotation, although minimised, results in visible segmental rotation in the laterally flexed
position.
Descriptive statistics were used to inspect the data for the direction and extent of NP
deformation, in addition to lateral flexion and rotation range at lumbar levels: L1-2 to
L5-S1. Direction of NP deformation in response to posture and segmental level was also
recorded. Unpaired t-tests were used to determine whether a gender difference in
flexibility was present. The NP position in neutral and lateral flexion was compared
using a paired t-test. Differences in lateral flexion angles between levels were examined
using ANOVA. Finally, simple linear regression was used to test for associations
between i) segmental lateral flexion and ii) NP deformation and lateral flexion. In all
statistical tests a probability of p<0.05 was used as the criterion to record significant
differences.
Chapter 6: The lateral flexion cohort study
Page VI-7
6.4 Results
There was no difference between genders for lateral flexion range of motion (p=0.47)
therefore data were pooled for subsequent analyses. A summary of the results for side
flexion, coincident rotation, and the extent and direction of the NP deformation for L1-2
to L5-S1 segmental levels, is provided in Table 6.1. In 95% of all cases a right sided NP
deformation occurred in response to end-range left side flexion, the exceptions were
found primarily at L5-S1.
There was a significant difference at all segmental levels contrasting the NP pixel
intensity position adopted in the side flexion compared with neutral axial images
(p<0.001) (Figure 6.4). The most pronounced change in the deformation of the nucleus
position was recorded for L2-3, L3-4 and L4-5 (Figure 6.4). There was a moderate
association between the magnitude of side-flexion and NP deformation only at L2-3
(r=0.54, p<0.01) (Table 6.1).
The greatest side flexion range was demonstrated at L3-4 and L4-5 (Figure 6.4) which
were significantly different from other adjacent levels (p<0.005). Coincident rotation
was small in contrast and showed no association with side flexion range (Figure 6.4).
Table 6.1: Summary of lumbar mobility and internal disc deformation responses to
sustained left side flexion in healthy volunteers
L1-2 L2-3 L3-4 L4-5 L5-S1
Side bend (°)
Mean (SD)
5.2 (2.24) 6.7 (2.22) 6.7 (1.64) 6.7 (3.48) 5.4 (3.86)
Rotation (°)
Mean (SD)
0.01 (1.97) 0.96 (2.13) 0.38 (1.74) 0.24 (2.07) 0.68 (2.78)
NP deformation
(percentage)
11.3
(9.75)
18.2
(11.0)
22.5
(7.1)
22.1
(7.95)
7.9
(9.86)
NP direction
(percentage)
21/21
(100%)
20/21
(95%)
21/21
(100%)
21/21
(100%)
18/21
(81%)
The apical segments showed the greatest displacement of the NP which was mirrored in
part by the relative extent of side-flexion. There were no associations between NP
deformation and the segmental axial rotation.
Chapter 6: The lateral flexion cohort study
Page VI-8
Figure 6.4: Inter-relationships between segmental side-flexion, coincident rotation and
the extent of NP deformation following unilateral sustained left side flexion position.
Marked change occurred in the apical segments.
6.5 Discussion
This study, involving young, asymptomatic subjects, sought to quantify NP deformation
in response to side flexion and to examine side flexion and segmental rotation range
relative to a lateral NP deformation.
The results showed a strong correlation between direction of NP deformation and
direction of lateral flexion, with 95% of segments (100/105) deforming towards the
contralateral side of lateral flexion. The directional relationship between NP
deformation and lateral flexion was expected to be strong, assuming a predictable
hydrostatic behaviour of the NP as it attenuates load in the healthy disc (Adams et al.,
1994). It was of interest to note that five IVDs deformed towards the side of lateral
flexion. Four of these occurred at L5-S1, where smaller ranges of lateral flexion were
recorded (mean: 5.4°), and one at L2-3.
From the MRI assessment, there was a significant shift of NP signal intensity away
from the neutral position away the direction of side bending, with a mean deformation
of 22.5%. There was a significant correlation between the magnitude of NP
deformation and range of lateral flexion at L2-3.
T2-weighted MRI images have been used to map NP hydration profiles in response to
changes in spinal posture. Pixel histograms of single (Edmondston et al., 2000) or
Chapter 6: The lateral flexion cohort study
Page VI-9
averaged data (Fazey et al., 2006) have elaborated the putative effect of postural
adaptations on IVD hydrostatic behaviour.
Hydration, and therefore signal intensity, as represented from T2-weighted images is
not uniform across the IVD or even within the NP. Methods of measuring pixel
intensity from a single sample across the IVD may be relatively insensitive to the
overall hydration change, particularly if the sampling profiles are not representative of
the IVD.
The greatest range of lateral flexion range occurred at the apex of the lateral curve, L2-
3, L3-4, and the least at the upper and lower limits of the curve. Studies by Pearcy et al
(Pearcy et al., 1984a; Pearcy et al., 1984b), using biplanar radiography of volunteers in
erect standing, have reported smaller segmental ranges of motion in lateral flexion than
the current study but greater ranges at L5-S1 and L1-2. This difference may reflect
supine positioning within the confines of the MRI in which the pelvis and lower limbs
were stabilised while lateral flexion was induced via shoulder and thoracic spine
movement. Such positioning may potentially limit the available range at the
lumbosacral junction and upper lumbar spine. Additionally, there is a tendency for the
spine to demonstrate a correction to neutral at the curve inflexion points which lie close
to the transitional levels. This phenomenon is illustrated in a balanced thoracolumbar
scoliosis curve where the inflexion vertebrae show a neutral disc alignment.
Segmental rotation ranges were small by comparison to previous studies (Pearcy et al.,
1984b). This finding most likely reflects subject positioning into lateral flexion where
rotation was only a secondary response. Care should be taken not to over interpret these
findings with respect to coupling patterns given the constrained nature of the
positioning used in the present study. Reports of associations between coronal and axial
plane motion provide no consensus as to the directional influence of one motion over
the other (Legaspi et al., 2007).
There are a number of limitations to this study which have the potential to influence the
interpretation of these data. Measurement errors may arise with the small ranges of
lateral flexion and NP deformation, particularly at L5-S1, and the relative initial resting
position of the NP. However, repeated assessment showed acceptable accuracy.
Chapter 6: The lateral flexion cohort study
Page VI-10
Additionally, it is known that 20-25% of the population demonstrate evidence of mild
physiological scoliosis (Grivas et al., 2008). A pre-existing degree of scoliosis would
inevitably influence both the NP position in neutral, and the potential range of both
lateral flexion and axial rotation. Available side flexion range may be compromised due
to the coupled rotation. It would be of interest to examine the influence of scoliosis in
future studies and map the association between NP deformation and the magnitude of
the deformity.
There was no significant correlation between rotation range and NP deformation. This is
not unexpected given the small ranges of rotation demonstrated. Further elaboration of
this in future studies, where rotation was unconstrained, would help define the extent of
association between both elements of coupled motion.
This study was limited to young subjects with no history of back pain or macroscopic
degenerative change on MRI. Future studies could consider the response of anular
injury and degenerative changes of the IVD to end-range side bending and rotation
using this MRI based technique of hydration mapping.
The technique employed in the current study involved three line samples across the IVD
to integrate and average the assessment of directional NP deformation. More complex
3-D profile maps of the anulus and NP would confer an improved evaluation of
hydration patterns across the entire intervertebral disc (Haughton, 2006; Périé et al.,
2001) as illustrated in Figure 6.5.
It would be of interest to replicate this study in an open magnet MR imager, which
would permit both physiological axial loading and unconstrained lateral flexion. More
accurate consideration of conjunct rotation and coupling patterns would then be
possible.
Chapter 6: The lateral flexion cohort study
Page VI-11
Figure 6.5: Relatively symmetrical 3-D profile of the NP in neutral (right) in contrast to
the profile derived in side flexion (left). Surface intensity plots of the NP emphasise the
displacement of the side flexed NP (left) away from the neutral position.
6.6 Conclusion
This study has demonstrated that the NP deforms in a predictable direction towards the
convexity in a laterally flexed lumbar spine. There was a significant degree of change in
NP hydration pattern between the neutral and laterally flexed position, most pronounced
at the mid lumbar levels and less so at L1-2 and L5-S1. The degree to which the NP
deforms generally correlates with the degree of segmental lateral flexion. Axial rotation,
occurring concomitantly with primary lateral flexion, did not correlate with NP
deformation or lateral flexion range. In this study physiological coupling patterns of the
lumbar segments cannot be inferred as side flexion was constrained.
Chapter 6: The lateral flexion cohort study
Page VI-12
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Adams M, McNally D, Chinn H, Dolan P. Posture and the compressive strength of the
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Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar
intradiscal deformation during flexion and extension by mathematical analysis
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Burnett AF, Barrett CJ, Marshall RN, Elliott BC, Day RE. Three-dimensional
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Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,
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Fennell A, Jones A, Hukins D. Migration of the nucleus pulposus within the
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Grivas TB, Vasiliadis ES, Mihas C, Triantafyllopoulos G, Kaspiris A. Trunk asymmetry
in juveniles. Scoliosis 2008; 3: 13.
Haughton V. Imaging intervertebral disc degeneration. J Bone Joint Surg Am 2006; 88
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Pearcy M, Portek I, Shepherd J. Three-dimensional x-ray analysis of normal movement
in the lumbar spine. Spine 1984a; 9(3): 294-7.
Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine
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Scannell JP, McGill SM. Disc prolapse: evidence of reversal with repeated extension.
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Scholten P, Veldhuizen A. The influence of spine geometry on the coupling between
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Chapter 6: The lateral flexion cohort study
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1990.
CHAPTER 7
Page VII-1
The older cohort MRI study
7.1 Summary
Intervertebral disc (IVD) degeneration is common and associated with age. Increased
ranges of lumbar intersegmental rotation have been associated with IVD degeneration.
Nucleus pulposus (NP) deformation in response to offset compressive loading has been
reported in flexed, extended and rotated postures. However, predictability of
deformation direction is uncertain in the presence of degeneration. The aim of this study
was to measure the magnitude and determine the direction and predictability of in vivo
lumbar NP deformation in older subjects placed in a rotated position within an MRI
scanner.
Eleven healthy subjects (5 female, 6 male) with a mean age of 48.4 (range: 40 – 57)
were imaged in neutral then left rotated postures employing mid-disc axial T2 and
coronal T1 weighted image sequences from L1-2 to L5-S1. Images were analysed for
direction and magnitude of NP deformation relative to rotation using a pixel profiling
technique, then compared with stage of IVD degeneration, and direction and angle of
concomitant segmental lateral flexion.
Mean NP deformation was 2.1% of disc width. At L3-4 there was a modest association
between lateral flexion and NP deformation (r=0.38, p<0.034). In the left rotation
position 47.3% of all discs deformed to the left and 52.7% to the right; 61.8% deformed
contralateral to the direction of intersegmental lateral flexion. NP deformation direction
was independent of level, grade of degeneration or segmental lateral flexion range.
In older subjects the direction of nucleus deformation was unpredictable relative to
rotation and poorly predictable relative to lateral flexion direction. The degree of
degeneration did not appear to be associated with predicting the deformation direction.
Chapter 7: The older cohort study
Page VII-2
7.2 Introduction
Degenerative or age related changes are prevalent in the lumbar spine, affecting 31% of
15 year olds (Salminen et al., 1993) and 100% of 50 year olds (Adams et al., 2002).
Lower lumbar segments typically show a greater extent of degenerative changes.
Biomechanically, moderate degenerative change has been demonstrated to be associated
with increased ranges of intersegmental rotation in the lumbar spine and severe
degeneration with decreased range (Haughton et al., 2002; Johansen et al., 1999).
Degeneration was putatively related to torsional strain by Farfan (Farfan et al., 1970)
who noted that anular lesions induced experimentally by torsion in cadaver spines were
identical in nature to those seen in degenerated discs. Farfan et al therefore hypothesised
that: degeneration was related more with rotational rather than compressive forces in
vivo, and that the greater ranges of intersegmental rotation seen at degenerated levels
compared with non degenerated levels may be interpreted as causative.
The pathophysiology of degeneration has been extensively studied and reviewed
(Hadjipavlou et al., 2008). It has a complex and multifactorial aetiology across the
spectrum of age, genetics, nutrition, metabolic, infection and mechanical influences.
This process of degeneration may precipitate anular tears and disc herniation which
disrupt the intradiscal environment and result in reduced capacity to attenuate
compressive load via the nucleus pulposus (NP) (Adams et al., 2010).
Magnetic Resonance imaging has been used to grade fluid loss and end plate changes
by analysis of T2 weighted signal changes with reference to normals (Jensen et al.,
2009; Jensen et al., 2008; Luoma et al., 2001).
Signal strength on T2 weighted MR images has been shown to be an accurate method
for assessing IVD hydration and potentially a more accurate measure of disc
degeneration than disc height (Haughton, 2006; Luoma et al., 2001).
It has been speculated that NP migration direction, a normal response to offset
compressive loading, is not consistent in sagittal plane postures of the lumbar spine
(Edmondston et al., 2000). However, there is preliminary in vivo evidence for
directionality of deformation in young normal lumbar spines positioned supine in left
rotation, albeit combined with flexion or extension (Fazey et al., 2006). No evidence
exists for the direction, magnitude or predictability of NP deformation in response to
rotated positions in the lumbar spines of older subjects.
Chapter 7: The older cohort study
Page VII-3
The purpose of this study was to measure the magnitude and determine the direction
and predictability of in vivo NP deformation using MRI in middle aged subjects
positioned into a rotated posture. It was hypothesised that greater intersegment lateral
flexion would induce the largest NP deformation from the neutral position; that more
severe disc degeneration would reduce the extent of NP deformation following axial or
coronal plane positioning and that the NP would deform contralaterally to the direction
of segmental lateral flexion.
7.3 Methods
11 healthy volunteers were recruited to the study; five female and six male with a mean
age of 48.4 years (range: 40 – 57). Exclusion criteria included general contraindications
to MRI and troublesome back pain requiring treatment within the past 12 months.
Written consent from each subject and institutional ethics approval were obtained.
Subjects were positioned on the gantry of a 1.5T MRI unit (Siemens, Berlin, Germany)
in supine followed by left rotated positions. A series of T2 weighted sagittal, axial and
T1 coronal image sequences were acquired. Axial T2 weighted neutral images were
obtained through the mid-disc region from L1-2 to L5-S1 using a fast spin echo
sequence (TR/TE [3020/102.0], field of view 20.9x16.7cm, 306x384 matrix, 4mm slice
thickness).
Coronal T1 weighted images were also obtained at each candidate level with a fast spin
echo sequence (TR/TE [619.0/11.0], field of view 30x30cm, 448x448 matrix, 4mm
slice thickness). The coronal slices were oriented orthogonal to the axial slices for each
imaged level.
Following acquisition in the neutral position the subjects were repositioned into left
trunk rotation by the placement of a dense foam cushion wedge under the left
hemipelvis and image sequences repeated (Figure 7.1).
7.3.1 Image analysis
Direction and magnitude of lateral flexion at each level was determined from coronal
T1 weighted MR images in the rotated position by placing a line of best fit across the
superior and inferior vertebral body end-plates of each intervertebral level. Image
Chapter 7: The older cohort study
Page VII-4
analysis software (NIH Image-J, Bethesda, USA) was used to measure the lateral
flexion angle.
Figure 7.1: Subject positioning on the gantry of the Magnetic Resonance imager. A
high density foam wedge cushion (arrow) under the left hemipelvis induces left lumbar
rotation
Coronal plane NP deformation was determined from analysis of pixel intensity using a
modification to a previously reported technique (Fazey et al., 2006) and Image-J
software. On each neutral and left rotated mid disc T2 weighted axial image three lines
were placed horizontally from right to left (Figure 7.2A). Raw pixel data from each set
of lines were normalised to 100 points and averaged (Figure 7.2B) within a Labview
routine (National Instruments, Austin, USA).
Segmental rotation angles, Ø, were derived from axial images as the angle subtended at
the intersection of a line extending through the mid disc and interlaminar points and the
horizontal image border (Figure 7.2C). Intersegmental rotation angles were taken as the
difference between the segmental angles of the respective subjacent segments.
Processed data were imported into Excel (Microsoft Corporation, Redmond, USA)
where magnitude and direction of NP deformation were assessed. As movement of the
isolated peak pixel point may not represent general fluid shift, total pixel numbers either
side of the 50th
percentile of the normalised averaged profiles were used to calculate
direction and percentage of NP hydration offset. This offset was derived for the neutral
resting position and compared with that from the rotated position; the difference
expressed as a percentage.
Chapter 7: The older cohort study
Page VII-5
Figure 7.2: Pixel numbers are averaged from three samples across the mid disc region
(A) on axial T2 weighted images from which hydration profiles (B) are derived to
calculate direction and extent of NP deformation. Note peak pixel point may not
represent magnitude of entire NP signal shift (B). Segmental rotation measured by the
angle (Ø) subtended between a line through the interlamina region and the centre of the
vertebral body with the image border (C). Subtraction of the derived angle from that of
the level below produced the intersegmental rotation angle (Ø).
Each disc was graded and classified by an experienced MRI radiologist (SS) on a 4
point scale from T2 weighted sagittal images as either: normal, mild, moderate or
severely degenerated. Grade was based upon the presence of osteophytes, disc height,
disc bulging and signal intensity.
All angle based measures demonstrated acceptable repeat reliability over 10 occasions
on a single image with coefficients of variation (CV) of between 1 – 3.7%. CV for NP
deformation percentage was <3%.
7.3.2 Data analysis
Descriptive statistics were used to inspect data recorded for NP deformation direction
and magnitude. Data were also evaluated for any directional relationship between NP
deformation and segmental lateral flexion range using least squares linear regression.
Comparisons were made between intervertebral levels and between subjects. A
probability of p<0.05 was used as the criterion to define meaningful differences.
7.4 Results
The mean NP deformation in the left rotated position across all subjects was 2.1%
(range: 0.1 – 6.3). By gender the mean percentages of NP deformation were 2.4%
(range: 0.1 – 6.3) and 1.8% (range: 0.2 – 4.3) for males and females respectively (Table
7.1).
Chapter 7: The older cohort study
Page VII-6
Table 7.1: Percentage NP deformation by intervertebral level
Subject 1
2 3 4 5 6 7 8 9 10 11 mean SD range
Gender F
M M M M F M F M F F
Age 55
46 40 50 48 54 48 46 57 47 41 48.4 5.4 40 – 57
L1-2 *
0.92 2.54 2.27 6.02 1.84 2.56 0.13 1.94 2.78 0.46 1.95 1.64 0.13 – 6.02
L2-3 4.27
4.75 0.23 4.65 1.84 1.35 0.51 1.12 3.69 2.03 3.42 2.53 1.68 0.23 – 4.65
L3-4 0.29
2.63 1.68 2.11 1.58 2.93 0.33 0.82 2.58 3.48 1.63 1.82 1.05 0.29 – 3.48
L4-5 0.17
1.47 0.89 6.35 5.29 3.34 0.5 0.84 0.07 0.84 4.16 2.17 2.22 0.07 – 6.35
L5-S1 1.49
3.88 1.9 3.92 2.75 0.48 1.0 3.53 1.49 2.57 0.38 2.13 1.29 0.38 – 3.92
* Scan series incomplete in this case. Data are degrees (°)
Chapter 7: The older cohort study
Page VII-7
Mean NP deformations by level and gender are represented in Figure 7.3. No difference
was noted between levels or genders with the exception of L1-2 where males
demonstrated smaller mean range of NP deformation. Deformation was greater at L2-3.
In the left rotated position the NP deformed towards the left in 26 (47.3%) and to the
right in 29 (52.7%) of discs.
Figure 7.3: Mean NP deformation represented by gender and intervertebral level. A
trend towards greater deformation at L2-3 is noted.
Mean intersegmental lateral flexion and rotation ranges for each intervertebral level are
reported in Table 7.2. In the left rotated position of the 55 segments assessed, segmental
lateral flexion occurred to the left on 32 occasions and to the right on 23 (Table 7.2).
There were no intervertebral level trends for segmental lateral flexion direction apart
from a modest correlation between intersegmental lateral flexion and NP deformation at
L3-4 [r=0.382, p=0.034] (Figure 7.4).
From the pixel profiling in the resting supine position, all cases showed the hydration
offset to be within 10% of the 50th
percentile (mean: 3.37%, range: 0 – 9.8). The NP
hydration offset in the resting position was right of the 50th
percentile of linear IVD
width in 67.3% of cases and to the left in 32.7%.
Chapter 7: The older cohort study
Page VII-8
Figure 7.4: A summary of the associations indexed by intervertebral level between
segmental rotation, coincident lateral flexion and NP deformation in the left rotation
position.
Table 7.2: Intersegmental lateral flexion and rotation absolute mean angles and
direction (number of cases) in the left rotated position
Level L1 – 2 L2 – 3 L3 – 4 L4 – 5 L5 – S1
Mean LF° 3.3 3.8 3.7 3.1 2.7
Mean Rot° 1.7 1.8 2.2 2.5 2.5
Left 7 5 5 8 7
Right 4 6 6 3 3
The direction of NP deformation relative to the direction of segmental lateral flexion is
shown in Table 7.2. In total 34/55 (61.8%) deformed to the contralateral side.
The NP deformed to the left more often in males (63.3%) than females (28%). Males
disc NPs also deformed contralaterally more often (70%) than those of female discs
(52%) (Figure 7.5).
Chapter 7: The older cohort study
Page VII-9
Figure 7.5: NP deformation relative to direction of segmental lateral flexion by gender
and intervertebral level. Contralateral direction is represented by grey and ipsilateral by
white.
Each level was inspected and graded for degenerative change. Grades of degeneration
and frequency of occurrence by intervertebral level are shown in table 7.3.
Table 7.3: Numbers of cases and grades of degeneration for all intervertebral levels
Level L1-2 L2-3 L3-4 L4-5 L5-S1
Normal 8 8 6 4 0
Mild 2 1 5 5 1
Moderate 1 2 0 2 7
Severe 0 0 0 0 3
Severely degenerated discs only occurred at L5-S1 (2 male; 1 female). Moderate
degeneration was found more frequently at every level except L3-4. No discs at L5-S1
were graded normal. There was no obvious relationship between the grade of
degeneration and percentage NP deformation at individual intervertebral levels. The
mean percentage NP deformation for each grade of degeneration being: normal, 2.17;
mild, 2.36; moderate, 1.94; severe, 2.11.
7.5 Discussion
This study is the first to report the direction and quantify the extent of NP deformation
in lumbar IVDs of older subjects placed in left rotation from the supine position. The
predictability of coronal plane deformation direction relative to rotation was low with
approximately half deforming to either right or left. The hypothesis that larger lateral
Chapter 7: The older cohort study
Page VII-10
flexion angles would correspond with increased NP deformation magnitude is not
supported by the present study apart from a modest association at L3-4. The hypothesis
that higher grades of degeneration would reduce the extent of NP deformation is not
supported as similar deformation magnitudes were seen across all grades of
degeneration. Additionally the hypothesis that NP deformation direction would occur
contralateral to the direction of lateral flexion was supported in 61.8% of IVDs.
The extent of NP deformation is less than previously reported in younger female
subjects by approximately 50% (Fazey et al., 2006) although this study employed
combined sagittal and axial plane subject positioning rather than in the isolated axial
plane as in the present study.
Previous reports suggesting reduced predictability of NP deformation behaviour in the
presence of degenerative change focussed only on sagittal plane postures (Brault et al.,
1997; Edmondston et al., 2000). As most studies, including the present, report variable
response and some degree of inconsistency it is reasonable to assume that this is a
common feature. While Edmondston et al (2000) suggested that degenerative change
may contribute to inconsistency that study did not find that such a variation was
exclusive to degenerated IVDs. Other authors have described inconsistent NP
directional behaviour in abnormal discs but did not define degeneration stage (Beattie et
al., 1994; Brault et al., 1997).
As degeneration results in loss of NP load bearing capability and increased anular
loading (Adams et al., 1996) it is likely assumed that this must influence the hydrostatic
properties of the IVD. A number of other factors may contribute: reduced proteoglycan
content, and therefore water holding capacity, is accompanied by increased collagen and
other structural changes (Hadjipavlou et al., 2008). As hydrostatic behaviour is peculiar
to fluids then areas of non fluid structure would be expected to behave differently. As
the degenerated IVD tends to exhibit irregular hydration signal on T2 weighted MR
images (Figure 7.6) it can be hypothesised that only the hydrated areas will behave
hydrostatically. Imaging and subsequent analysis that attempts to characterise behaviour
of the entire IVD may therefore reveal areas that do not behave in such a characteristic
manner.
Distribution of degenerative grades across intervertebral levels was generally as
expected given the inclusion of all lumbar levels and a trend for subject ages towards
the lower end of the reported range.
Chapter 7: The older cohort study
Page VII-11
Figure 7.6: Three dimensional representation of hydration profile showing relative
difference in signal strength between normal L4-5 IVD of a 24 year old male (A) and
degenerated L5-S1 IVD of a 48 year old male (B). Note the patchy hydration profile in
B.
Any correlation between NP deformation and lateral flexion range would be expected to
be positive given the normal fluid mechanics of a well hydrated IVD. Deformation of
fluid based compounds within the disc typically occurs from an area of high to low
compression. The expectation that the NP will always deform away from an area of
compressive force does not consider internal pressure gradients. While intradiscal
pressures have been reported they are static and typically derived from pressure
transducer readings in the mid-disc region (Nachemson, 1960; Sato et al., 1999; Wilke
et al., 1999). It may be hypothesised that if unilateral tensile force exceeds compressive
force on the opposite side then net NP deformation would occur towards the side of
compression rather than away. This theory would require an intact anulus and may
explain variations in directional trends of the NP in normal IVDs.
Studies of intradiscal pressure relative to rotation report only compressive force within
the disc (van Deursen et al., 2001; Wilke et al., 1996; Yantzer et al., 2007). In vivo
studies to differentiate tensile and compressive force influences on the IVD would be
technically difficult but may be feasible within a suitable animal model.
Chapter 7: The older cohort study
Page VII-12
7.6 Limitations
This study was limited to a sample of 11 subjects. Although each lumbar level was
imaged and analysed for NP deformation patterns, comparison within and between
intervertebral levels a larger sample size may be more revealing of trends.
Gender differences noted in both laterality of NP deformation and direction relative to
both lateral flexion and rotation may be an effect of sample size rather than true gender
differences as these have not been reported relative to IVD geometry (Farfan et al.,
1972).
The non weightbearing, unidirectional subject positioning in the present study restricts
the ability to relate these observations to functional behaviour of the spine.
Averaging data from three samples across each IVD, a more extensive sampling method
than previous reports, (Alexander et al., 2007; Brault et al., 1997; Edmondston et al.,
2000) may still not accurately represent the hydration pattern within the entire IVD.
7.7 Future studies
Farfan reported the influence of disc geometry on the pattern of disc degeneration and
anular tears concluding that disc shape and articular process symmetry were relative
(Farfan et al., 1972). It may be that such geometrical variants also influence NP
deformation patterns through changes in the anular constraint patterns of the NP. While
the original studies were post mortem the advent of multiplanar and three dimensional
imaging using weightbearing MRI would allow such studies to be performed in vivo.
Replication of the present study with larger subject numbers and a cohort of younger
adult subjects would facilitate comparisons.
7.8 Conclusion
Lumbar NP deformation direction in older subjects positioned in left rotation is not
predictable. Deformation direction relative to intersegmental lateral flexion direction
showed a trend towards the contralateral side. No consistent relationship was found
between mean NP deformation and intersegmental lateral flexion angles.
Chapter 7: The older cohort study
Page VII-13
References
Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain. London,:
Churchill Livingstone, 2002.
Adams MA, McNally DS, Dolan P. 'Stress' distributions inside intervertebral discs: the
effects of age and degeneration. The Journal of Bone and Joint Surgery Br 1996;
78(6): 965-72.
Adams MA, Stefanakis M, Dolan P. Healing of a painful intervertebral disc should not
be confused with reversing disc degeneration: implications for physical therapies
for discogenic back pain. Clin Biomech (Bristol, Avon) 2010; 25(10): 961-71.
Alexander LA, Hancock E, Agouris I, Smith FW, MacSween A. The response of the
nucleus pulposus of the lumbar intervertebral discs to functionally loaded
positions. Spine 2007; 32(14): 1508-12.
Beattie PF, Brooks W, Rothstein J. Effect of lordosis on the position of the nucleus
pulposus in supine subjects. Spine 1994; 19: 2096-102.
Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar
intradiscal deformation during flexion and extension by mathematical analysis
of magnetic resonance imaging pixel intensity profiles. Spine 1997; 22: 2066-
72.
Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,
Singer K. MRI evaluation of lumbar spine flexion and extension in
asymptomatic individuals. Manual Therapy 2000; 5: 158-64.
Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsion on
the lumbar intervertebral joints: the role of torsion in the production of disc
degeneration. J Bone Joint Surg Am 1970; 52(3): 468-97.
Farfan HF, Huberdeau RM, Dubow HI. Lumbar intervertebral disc degeneration: the
influence of geometrical features on the pattern of disc degeneration - a post
mortem study. J Bone Joint Surg Am 1972; 54(3): 492-510.
Fazey P, Song S, Mønsas A, Johansson L, Haukalid T, Price R, Singer K. An MRI
investigation of intervertebral disc deformation in response to torsion. Clinical
Biomechanics 2006; 21: 538-42.
Hadjipavlou AG, Tzermiadianos MN, Bogduk N, Zindrick MR. The pathophysiology of
disc degeneration: a critical review. J Bone Joint Surg Br 2008; 90(10): 1261-70.
Haughton V. Imaging intervertebral disc degeneration. J Bone Joint Surg Am 2006; 88
Suppl 2: 15-20.
Haughton V, Rogers B, Meyerand M, Resnick D. Measuring the axial rotation of
lumbar vertebrae in vivo with MR imaging. American Journal of
Neuroradiology 2002; 23: 1110-6.
Jensen TS, Bendix T, Sorensen JS, Manniche C, Korsholm L, Kjaer P. Characteristics
and natural course of vertebral endplate signal (Modic) changes in the Danish
general population. BMC Musculoskelet Disord 2009; 10: 81.
Jensen TS, Karppinen J, Sorensen JS, Niinimaki J, Leboeuf-Yde C. Vertebral endplate
signal changes (Modic change): a systematic literature review of prevalence and
association with non-specific low back pain. Eur Spine J 2008; 17(11): 1407-22.
Johansen JG, Nork M, Grand F. Torsional instability of the lumbar spine. Rivista di
Neuroradiologia 1999; 12: 193-5.
Luoma K, Vehmas T, Riihimaki H, Raininko R. Disc height and signal intensity of the
nucleus pulposus on magnetic resonance imaging as indicators of lumbar disc
degeneration. Spine 2001; 26(6): 680-6.
Nachemson A. Lumbar intradiscal pressure. Acta Orthopaedica Scandinavica,
Supplementum 1960; 43: 1-104.
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Page VII-14
Salminen JJ, Erkintalo-Tertti MO, Paajanen HE. Magnetic resonance imaging findings
of lumbar spine in the young: correlation with leisure time physical activity,
spinal mobility, and trunk muscle strength in 15-year-old pupils with or without
low-back pain. J Spinal Disord 1993; 6(5): 386-91.
Sato KMDD, Kikuchi SMDD, Yonezawa TMD. In Vivo Intradiscal Pressure
Measurement in Healthy Individuals and in Patients With Ongoing Back
Problems. Spine 1999; 24(23): 2468-74.
van Deursen D, Snijders C, van Dieën J, Kingma I, van Deursen L. The effect of
passive vertebral rotation on pressure in the nucleus pulposus. Journal of
Biomechanics 2001; 34: 405- 8.
Wilke HJ, Neef P, Caimi M, Hoogland T, Claes LE. New in vivo measurements of
pressures in the intervertebral disc in daily life. Spine 1999; 24(8): 755-62.
Wilke HJ, Wolf S, Claes LE, Arand M, Wiesend A. Influence of varying muscle forces
on lumbar intradiscal pressure: an in vitro study. J Biomech 1996; 29(4): 549-
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Yantzer BK, Freeman TB, Lee WE, 3rd, Nichols T, Inamasu J, Guiot B, Johnson WM.
Torsion-induced pressure distribution changes in human intervertebral discs: an
in vitro study. Spine 2007; 32(8): 881-4.
CHAPTER 8
Page VIII-1
The scoliosis cohort MRI study
8.1 Summary
Scoliosis reflects morphological changes to the vertebral elements and compensatory
wedging of the intervertebral bodies and discs with exaggerated axial, sagittal and
coronal spinal alignment. The purpose of this study was to provide a detailed
assessment of the hydration distribution within the nucleus pulposus (NP) of the lumbar
intervertebral disc in scoliosis cases.
Twelve cases of adolescent scoliosis were assessed with MRI as part of a routine pre-
surgical workup. Thoracic and lumbar image sequences were used to derive the Cobb
angle and the apical disc wedge angle. The extent of any coronal plane nucleus
deformation was measured using a hydration profiling technique.
Lumbar Cobb angles ranged from 12.4° to 54.6°, with a mean of 34.9°. Intersegmental
rotation at the apex ranged from 0.8° to 8.0°, with a mean of 4.6°. Segmental lateral
flexion ranged from 4.2° to 13.7°, with a mean of 7.5°. The apical NP showed an offset
away from the midline which was weakly associated with the extent of the Cobb angle
(r=0.12).
Adolescent lumbar compensatory scoliosis results in exaggeration of the three cardinal
planes which coupled with disc wedging contribute to an offset deformation of the NP
away from the compressive axis. In general, the greater the disc wedging and lumbar
Cobb angles the further the displacement of the NP.
Chapter 8: The scoliosis study
Page VIII-2
8.2 Introduction
Idiopathic scoliosis affects 2%-3% of children aged between 10 and 16 years (Reamy &
Slakey, 2001) with females representing 90% of cases with Cobb angles >30°. Scoliosis
is a tri-dimensional phenomenon with deformity components involving axial, coronal
and sagittal planes. In 90% of cases the primary curvature convexity is to the right and
where a compensatory lumbar curve exists, a left convexity is found in 70% of cases.
A major focus of the literature concerns the coronal plane deformity, exemplified by the
Cobb angle measurement (Cobb, 1948), with relatively less consideration of the axial
plane component. Fewer studies yet have considered the effect of scoliosis on the
intervertebral disc (IVD) and the extent to which the nucleus pulposus (NP) is deformed
in relation to the magnitude of the secondary lumbar curve. Périé (Périé et al., 2003) has
reported three dimensional mathematical modelling of NP using Magnetic Resonance
Imaging (MRI) in primary thoracic idiopathic scoliosis. Although NP deformation is
reported it is not quantified. Violas (Violas et al., 2007a; b) proposed a similar three
dimensional reconstruction of the NP in secondary lumbar scoliotic curves and
calculated a volume ratio between NP and the entire disc. Although this ratio reflects
relative tissue hydration there was no assessment of variations within the NP. Further,
the extent of NP deformation was not quantified.
Traditional imaging of scoliosis relies upon plain posterior-anterior (PA) radiographs
from which Cobb angles are derived and curve progression can be monitored; an
approach restricting this assessment to two dimensions. Computerised tomography (CT)
and MRI provide an accurate way of imaging the scoliotic spine, resulting in a greater
understanding of the tri-dimensional nature of the condition (Wright, 2000). MRI is
typically used to exclude occult neurological pathology such as hydromyelia,
syringomyelia and tethered cord (Wright, 2000). MRI may also enable characterisation
of NP deformation direction and magnitude as a result of the deformity.
Nucleus pulposus deformation in the lumbar region has been documented using MRI in
healthy cases, relative to subject positioning in the sagittal (Beattie et al., 1994;
Edmondston et al., 2000; Fennell et al., 1996), coronal (Fazey et al., 2010) and axial
planes (Fazey et al., 2006). The consistent trend has been to observe in the majority of
cases, an offset deformation of the NP away from the area of greatest compression. In
sagittal plane flexion the NP adopts a posterior locus; in side flexion a locus to the
Chapter 8: The scoliosis study
Page VIII-3
convexity of the posture and, in rotation a mixed position that combines the effect of
axial and side-flexed load upon the intervertebral disc (IVD).
Axial rotation, measured with a variety of two and three dimensional methods (Vrtovec
et al., 2009), provides quantitative information on surgical or conservative management
results (Pinheiro et al., 2009), where correction to a more neutral alignment is the
objective. Axial rotation at the apex of the lumbar curvature can be used to reliably
predict post operative coronal spinal decompensation (Behensky et al., 2007).
Coronal plane deformity is evaluated routinely using the method described by Cobb
and may be applied to both primary thoracic and secondary lumbar curves. A regional
assessment of curvature is achieved in the coronal plane which integrates the effect of
disc and vertebral body wedging. Intersegmental angles which contribute to the
deformity are rarely reported (Wright, 2000).
Axial rotation in scoliosis is an integral component of the deformity and has been
shown to occur in both the IVD and the vertebral body. Up to 55% of axial deformation
in scoliosis has been attributed to torsion of the IVD (Birchall et al., 2005). Wedging
also occurs mainly in the IVD with the vertebral body accorded only 22% of the
asymmetry (Beuerlein et al., 2003). Coupling of axial and coronal plane motion in the
spine occurs physiologically, although these relationships have not been investigated
definitively (Panjabi, 1989). Lateral bending of the scoliotic spine does not induce
coupled axial rotation either in primary thoracic or secondary lumbar curves at the apex
(Beuerlein et al., 2003). No studies to date have considered, in the lumbar region of
scoliotic spines, the association between NP deformation and the degree of
intersegmental coronal plane wedging or intersegmental rotation angle. The purpose of
this MRI study was to quantify NP deformation in secondary lumbar curvature of
subjects with scoliosis and to consider the association between IVD wedge angulation
and NP offset using a method developed specifically for a lumbar spine model.
8.3 Methods
Preoperative magnetic resonance images and plain radiographs were obtained
retrospectively for 14 subjects; 2 male and 12 female, with a mean age of 13.5 years
(range: 12-19).
Subjects were identified by three spinal deformity surgeons (PW, EM and DD) as
potential candidates for corrective surgery and had undergone routine pre-operative
Chapter 8: The scoliosis study
Page VIII-4
staging. This included standing plain P-A radiographs for Cobb angle measurement, and
coronal plus axial MRI sequences to exclude occult neurological pathology.
Subject selection criteria included presence of a secondary lumbar curve and availability
of T2 weighted axial MR screening images through the mid-disc region at the apex of
the lumbar curve. Over 100 archived cases were reviewed to determine those where
optimal T2-weighted lumbar images sequences were available for this sub-set
investigation. The most frequent reasons for exclusion were: Complete MRI sequences
unavailable – 55%, T2 weighted axial images through mid disc region unavailable –
35%.
Coronal plain radiographs were used to derive Cobb angles of the lumbar curvature
employing the method described by Cobb (Cobb, 1948) plus Dicom image analysis
software (Philips MxLiteView, Andover, USA). A line was placed along the superior
and inferior vertebral end plates defining the lumbar curve. The angle of intersection of
perpendicular lines subtended from each was recorded as the Cobb measurement.
Intersegmental lateral flexion angulation was measured in the coronal plane from MRI
images using the same image analysis software. Lines were inscribed along adjacent
end plates and the angle, θ, subtended by orthogonal extensions recorded as the
intersegmental lateral flexion angle in degrees (Figure 8.1A).
Segmental axial rotation was defined as the angle, Ø, subtended by the horizontal
image margin and a line drawn through the midpoint of the inter lamina region and the
spinous process (Figure 8.1B). Intersegmental angle was derived by subtracting the
segmental axial rotation of the cranial segment from that of the subjacent level of the
target motion segment. All angle based measures demonstrated acceptable intra-image
repeat reliability over 10 occasions with coefficients of variation of between 1-3.7%.
Direction of NP deformation was derived from the T2 weighted mid-disc axial images
at, plus adjacent to, the apex of the lumbar curve using a previously validated technique
(Fazey et al., 2006) and image analysis software (Image-J, NIH, Bethesda, USA). This
enabled pixel intensity profiling to represent the relative hydration pattern across the
disc. On axial images, 3 closely spaced parallel lines were placed across the mid-disc
region from right to left (Figure 8.2A). Pixel positions along each line were normalised
to 100 points and averaged using a Labview software routine (National Instruments,
Austin, USA) (Figure 8.2B). These data were imported into Excel where the direction
and magnitude of any offset of the NP profile was derived.
Chapter 8: The scoliosis study
Page VIII-5
Figure 8.1: Cobb methodology for calculation of segmental coronal plane angulation
(A). Segmental rotation (B) was measured by the angle subtended between a line
through the interlamina region and the centre of the vertebral body with the image
border. Subtraction of the result from that of the level below gives the intersegmental
rotation angle incorporating the target IVD.
Figure 8.2: NP deformation was measured from the mean pixel intensity of three lines
placed across the mid disc region of the apical IVD (A). These data were plotted and
averaged (B) to calculate NP hydration offset.
Descriptive statistics were used to report all data and linear regression used to inspect
relationships between direction and magnitude of NP deformation and intersegmental
lateral flexion and Cobb angles. A probability of p<0.05 defined a meaningful statistical
association.
Chapter 8: The scoliosis study
Page VIII-6
8.4 Results
As there was no gender difference in the NP deformation data, the cases were pooled for
all analyses. Results for intersegmental lateral flexion angles, inter segmental axial
rotation angles, NP deformation extent and lumbar Cobb angles, are shown in table 8.1.
The apical level varied between subjects, occurring most commonly at L2-3 (50%) with
T12-L1 the next most common (28%). In two cases the apex occurred at L1-2. In all
cases the NP deformed towards the convexity of the lumbar curve and away from the
intersegmental lateral flexion direction. Segmental axial rotation occurred in the same
direction as the concavity in all cases. Mean NP deformation was 17.5% (range: 0.6 –
58.7).
A weak relationship (r=0.1) was seen between lateral flexion segmental angulation
range and NP deformation magnitude. Similarly there was no relationship between
either NP deformation and lumbar cobb angles, or between NP deformation and
segmental rotation angles.
Table 8.1: Lumbar mobility and nucleus pulposus deformation in apical segments of
secondary lumbar curve of 14 subjects with scoliosis.
Mean SD Range
Lateral Flexion (°) 7.5 2.4 4.2 – 13.7
Segmental Rotation (°) 4.6 2.1 0.8 – 8.0
NP deformation (%) 17.5 13.8 0.6 – 58.7
Cobb (°) 34.9 13.7 12.4 – 54.6
Figure 8.3: Two dimensional coronal (A) and axial (B) T2 weighted magnetic
resonance images show hydration signal offset away from the concavity. The three
dimensional representation (C) highlights the offset and variation across the entire IVD.
8.5 Discussion
This study sought to quantify NP deformation relative to segmental axial rotation and
coronal plane angulation at the apex of secondary lumbar curvature in 14 adolescent
scoliosis cases.
A B C
Chapter 8: The scoliosis study
Page VIII-7
As expected, the results showed an association between the direction of NP deformation
and the direction of both the regional and segmental lateral flexion, with all NPs
deforming contralaterally and towards the convexity. While such a directional
relationship was anticipated given the hydrostatic nature of NP mechanics and
propensity for fluid shift away from offset compressive loading this has not always been
demonstrated. A previous study revealing a similar trend in normal subjects reported a
few cases (5%) where NP deformed towards the concavity (Fazey et al., 2010). This
tended to occur at non apical segments having smaller ranges of lateral flexion. The
stronger relationship in the present study may be attributable to generally larger ranges
of lateral flexion, particularly at the apical segments, and the effects of longstanding
structural deformity.
Structural and histochemical changes have been demonstrated specific to either the
convexity or concavity within the IVD. Consistent with the observed deformation,
Roberts et al (1993) reported reduced proteoglycan and water content in both the end-
plate and IVD, particularly on the concave side in scoliosis. While readily attributable to
offset compressive loading, such histochemical changes are also postulated to be
associated with curve progression (Roberts et al., 1993). Additionally, significantly
higher levels of collagen cross linking within the IVD on the convex side along with
increased metalloproteinases are presumed to represent increased matrix turnover and
tissue remodelling (Crean et al., 1997; Duance et al., 1998). It is unclear whether these
changes associated with deformity towards convexity are causative or a result of the
deformity.
There were only weak relationships between the magnitude of NP deformation and that
of the regional Cobb or segmental lateral flexion angles. While it could be reasonably
assumed that the magnitude of offset loading characterised by Cobb and/or segmental
lateral flexion angles relative to that of NP deformation would be predictable this has
never been reported. This weak relationship may be explained by the end range nature
of the deformity. Within an intact anulus the NP is constrained by the capsular function
of the inner anular fibres, when those on the convex side reach maximum tension no
further NP deformation towards that side is possible. Further small movements into
lateral flexion will gain increased segmental angulation due to fibre creep but still not
permit further deformation. On this basis a stronger relationship may be evident within
sub maximal lateral flexion ranges. It could also be postulated that if the tensile forces
in the anular fibres at the convexity exceed the compressive force then NP deformation
Chapter 8: The scoliosis study
Page VIII-8
could be ipsilateral to the offset compressive load. This observation has previously been
reported in a minority of subjects (Fazey et al., 2010).
There was no relationship between NP deformation magnitude and segmental rotation
angles. The related literature reports a directional relationship between NP deformation
and rotation but does not report its strength (Fazey et al., 2006). A stronger relationship
with between NP deformation and lateral flexion in normal subjects is postulated (Fazey
et al., 2006). The present study showed a strong directional relationship between
rotation and NP deformation direction but this is likely attributable to the consistent
ipsilateral direction of axial rotation and lateral flexion in scoliosis.
Though intersegmental rotation angles were small they were greater than those
previously reported in asymptomatic volunteers (Haughton et al., 2002; Pearcy &
Tibrewal, 1984). While these studies report intervertebral angles, results of the present
study may reflect additional rotary deformity within the vertebral body as well as the
IVD (Birchall et al., 2005). Subject positioning within the MRI may influence rotation
range. It is reported that supine positioning relaxes sagittal and coronal curves and
presumably axial rotation (Birchall et al., 1997; Torell et al., 1985) though this is
disputed (Ho et al., 1993). Future studies using a standing open magnet MRI would help
resolve the question.
The weak negative relationship between rotation and lateral flexion angles may suggest
greater ranges of rotation are possible in the presence of less lateral flexion. This is
consistent with the biomechanical principle that primary motion in one plane influences
available range in a subsequent plane (Pearcy & Hindle, 1991; White & Panjabi, 1990)
though this has not been reported relative to structural changes in scoliosis (Birchall et
al., 2005; Liljenqvist et al., 2002).
Previous studies measuring NP deformation have sought to quantify excursion of fluid
shifts by comparing measurements from a neutral starting position with those from a
subsequent posture, either flexion, rotation or lateral flexion (Edmondston et al., 2000;
Fazey et al., 2006; Fazey et al., 2010). In this study subjects were imaged in the resting
position only; therefore no quantification of further passive rotation was possible.
Resting position of the NP was assessed relative to the linear mid-position of lines
across the disc (Figure 8.2). This position is somewhat arbitrary as a truly neutral
positioning of the NP at rest would be rare (Fazey et al., 2010).
Scoliosis is frequently imaged with conventional plain radiographs in both the resting
and traction position to assess the degree of correction and potential management
Chapter 8: The scoliosis study
Page VIII-9
options. It would be of interest for future studies employing the same MRI
methodology to measure NP deformation in both resting and traction positions to
determine the relationship between magnitude of change in the two imaged positions.
This could be done both immediately and over time to test the ability of this
methodology to predict correction.
T2 weighted MRI is an elegant choice of modality to elucidate hydration profiles from
pixel intensity (Boos et al., 1994). Three dimensional image analysis would be optimal
for this purpose to elaborate the detail of hydration profiles (Figure 8.3).
Quantification of NP deformation in the lumbar curvature may also predict post
operative outcome or provide a reliable method to assess outcomes following
conservative management.
8.6 Limitations
This study was limited to a small number of subjects with idiopathic scoliosis of
sufficient magnitude to contemplate surgical intervention. Future studies should include
cases with lesser degrees of curvature and extend to other vertebral levels including the
primary thoracic curve. Positioning is known to influence curve size, therefore a
comparison with weightbearing in a standing MR imager would clarify the degree to
which position influences NP deformation. Comparisons between the methodology used
in the present study and three dimensional image analysis of the entire disc would
further elaborate the utility of such a method. The use of various disparate methods of
segmental rotation measurement applied to images may devalue comparisons with
reported ranges in the literature (Cassar-Pullicino & Eisenstein, 2002).
8.7 Conclusions
This study in subjects with idiopathic scoliosis has demonstrated that NP deforms
towards the side of convexity in the apex of secondary lumbar curves in a highly
predictable way. There was weak correlation between the degree of deformation and
segmental lateral flexion angulation or Cobb angle. No relationship was demonstrated
between NP deformation and intersegmental rotation angles.
Chapter 8: The scoliosis study
Page VIII-10
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Ho EK, Upadhyay SS, Chan FL, Hsu LC, Leong JC. New methods of measuring
vertebral rotation from computed tomographic scans. An intraobserver and
interobserver study on girls with scoliosis. Spine 1993; 18(9): 1173-7.
Liljenqvist UR, Allkemper T, Hackenberg L, Link TM, Steinbeck J, Halm HF. Analysis
of vertebral morphology in idiopathic scoliosis with use of magnetic resonance
imaging and multiplanar reconstruction. J Bone Joint Surg Am 2002; 84-A(3):
359-68.
Chapter 8: The scoliosis study
Page VIII-11
Panjabi M. How does posture affect coupling in the lumbar spine? Spine 1989; 14:
1002-11.
Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine
measured by three-dimensional radiography. Spine 1984; 9: 582-87.
Pearcy MJ, Hindle RJ. Axial rotation of lumbar intervertebral joints in forward flexion.
Proc Inst Mech Eng [H] 1991; 205(4): 205-9.
Périé D, Curnier D, de Gauzy JS. Correlation between nucleus zone migration within
scoliotic intervertebral discs and mechanical properties distribution within
scoliotic vertebrae. Magn Reson Imaging 2003; 21(9): 949-53.
Pinheiro AP, Tanure MC, Oliveira AS. Validity and reliability of a computer method to
estimate vertebral axial rotation from digital radiographs. Eur Spine J 2009.
Reamy BV, Slakey JB. Adolescent idiopathic scoliosis: review and current concepts.
Am Fam Physician 2001; 64(1): 111-6.
Roberts S, Menage J, Eisenstein SM. The cartilage end-plate and intervertebral disc in
scoliosis: calcification and other sequelae. J Orthop Res 1993; 11(5): 747-57.
Torell G, Nachemson A, Haderspeck-Grib K, Schultz A. Standing and supine Cobb
measures in girls with idiopathic scoliosis. Spine 1985; 10(5): 425-7.
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intervertebral disc volume properties using MRI in idiopathic scoliosis surgery.
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Violas P, Estivalezes E, Briot J, Sales de Gauzy J, Swider P. Quantification of
intervertebral disc volume properties below spine fusion, using magnetic
resonance imaging, in adolescent idiopathic scoliosis surgery. Spine 2007b;
32(15): E405-12.
Vrtovec T, Pernus F, Likar B. A review of methods for quantitative evaluation of spinal
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White A, Panjabi M. Clinical Biomechanics of the Spine, 2 ed. Philadelphia: Lippincott,
1990;
Wright N. Imaging in scoliosis. Arch Dis Child 2000; 82(1): 38-40.
CHAPTER 9
Page IX-1
The longitudinal case study
9.1 Summary
Rotation is a frequent mechanism by which the lumbar intervertebral disc (IVD) may be
injured resulting in herniation of the nucleus pulposus.
Conservative management of acute nucleus pulposus herniation is a common option and
produces comparable results to surgery. While there are numerous reports of
spontaneous resorption of extruded nuclear material few studies examine changes over
the longer term or report variables other than protrusion size.
A 32 year old woman with a large central herniated nucleus pulposus at L4-5 was
followed over a 12 year period with serial MRI from which thecal sac dimension, cross
sectional area and percentage fat infiltration of multifidus at L4-5 and L3-4 levels were
derived.
Antero-posterior (A-P) thecal sac dimension was restored as herniation size reduced.
The largest reduction occurring during the initial six months post injury. Cross sectional
area (CSA) of multifidus reduced bilaterally post injury and gradually recovered over
the length of the study period. Fat infiltration markedly increased bilaterally in the
initial six months and gradually reduced over the 12 year period to less than immediate
post injury values.
The natural history of a case of herniated nucleus pulposus demonstrated marked and
continued improvement in herniation size, fat infiltration, cross sectional area of
adjacent muscle and self reported functional capacity over 12 years.
Chapter 9: The longitudinal case study
Page IX-2
9.2 Introduction
Intervertebral disc (IVD) injury resulting in herniation of the nucleus pulposus (HNP) is
a common cause of low back pain (Adams et al., 2002). Incidence is increased in the
younger population (Kim et al., 2009) and has been associated with repetitive flexion
(Scannell et al., 2009) and rotational forces (Farfan et al., 1970). Local and/or distal
symptoms are a common sequel with or without altered peripheral neurological status.
Management has traditionally involved surgical options including microdiscectomy
however conservative management has increased in popularity and is reported to have at
least equal outcomes to surgery (Atlas et al., 2005; Singer et al., 2004). Choice of
management approach is often based on lifestyle and patient preference.
The natural course of herniated IVD is for regression of the degree of disc material
protrusion (Benoist, 2002; Cribb et al., 2007; Kobayashi et al., 2003), which has been
postulated to be due in part to resorption and shrinkage of the extruded material
following a complex process of neovascularisation, phagocytosis and immune response
(Autio et al., 2006; Benoist, 2002; Cribb et al., 2007). Numerous reports exist,
predominantly as case studies, of spontaneous resorption of HNP (Kobayashi et al.,
2003) and focus primarily on functional outcomes, symptoms and imaging changes in
the short to intermediate period after injury.
Few studies of HNP give consideration to the effect of injury on adjacent paraspinal
musculature with respect to changes relative to disc injury and the natural history of the
condition. Cross sectional area (CSA) and muscle morphology have been associated
with functional decline and can predispose to recurrence or ongoing symptoms (Hides
et al., 1996). Several authors have reported the CSA of various spinal muscles and their
changes over time relative to symptoms (Barker et al., 2004; Danneels et al., 2000;
Hides et al., 2008) using a variety of imaging techniques including MRI and
ultrasonography .
Acute and late change in muscle morphology, specifically infiltration by fatty tissue,
has been reportedly associated with spinal pain syndromes (Kjaer et al., 2007;
Mengiardi et al., 2006). A cause and effect relationship between fat infiltration and
dysfunction has not been established although it appears to affect the posterior
musculature while sparing anterior structures (Elliott et al., 2008).
In this report we describe the case of a 32 year old female who sustained a large central
L4-5 HNP and elected conservative management. Serial MRI scans over 12 years are
Chapter 9: The longitudinal case study
Page IX-3
presented along with evaluation of changes in CSA and fat infiltration of surrounding
musculature.
9.3 Case report
The patient presented with acute onset of low back pain with radiation to the left
buttock, posterior thigh and lateral leg to the ankle. Symptoms were precipitated by
repetitive bending, lifting and twisting while unloading 25kg boxes in a confined space.
On physical examination at three weeks following symptom onset, the patient reported
intolerance to sitting and frequent disturbance of sleep. Erect standing demonstrated a
trunk list to the right. All spinal movements were markedly restricted by pain. Forward
flexion was limited to fingertips reaching above the knees. Extension was <50%. In
supine lying there was marked restriction of Straight Leg Raise (SLR) bilaterally (45°),
with positive cross-over. Light touch sensation was impaired over the L5 distribution in
the posterolateral leg. Deep tendon reflexes were diminished at the patella and absent at
the achilles bilaterally. Lower limb perfusion was normal.
Plain radiographs demonstrated preexistent anterior osteophytes and loss of disc height
at L4-5. Computerised tomography at one week post injury revealed a large
posterocentral disc protrusion. The bony canal dimensions and adjacent disc levels were
normal. At four weeks post onset, lumbar MRI sequences confirmed the extent of the
herniation with migration of disc material inferior to the L5 superior end plate, causing
compression of the ventral aspect of the thecal sac (Figures 9.1A and 9.2). At this time
the patient received left epidural steroid injection at L4-5 under radiological guidance,
resulting in marked improvement in back and leg pain.
On review at eight weeks post injury, SLR remained at 45° left and 60° right. Standing
posture was normal. Following discussion the patient maintained a preference to
continue conservative management including physical therapy, hydrotherapy and anti-
inflammatory medications as required. Following initial improvement in symptoms for
three weeks, a recurrence of radicular symptoms and sleep disturbance necessitated a
second L4-5 epidural at 9 weeks resulting in significant symptom reduction. At this
time forward flexion was still limited by pain to fingertips reaching the knees; while
trunk extension was reduced to approximately 75% of the expected range for her age.
SLR increased to 60° on the left.
Chapter 9: The longitudinal case study
Page IX-4
A third epidural was administered at eight months following increased symptoms, again
with good symptomatic effect. Repeat MRI examination at six months demonstrated
marked reduction in the size of the central disc prolapse (Figures 9.1B and 9.2).
Figure 9.1: L4-5 axial T2(A) and T1(B) weighted images acquired in, from left to right,
1997, 1998, 2002 and 2009. Note marked reduction in central disc protrusion between
images taken in July 1997 and January 1998 – a period of six months, and gradual
resorption and reduction in subsequent images.
Figure 9.2: Serial sagittal T2 weighted images acquired, from left to right, in
1997,1998, 2002 and 2009 demonstrating encroachment of extruded disc material into
the spinal canal indenting the thecal sac. Early degenerative change is seen in L4-5 disc,
more marked in the image from 2009.
Chapter 9: The longitudinal case study
Page IX-5
On review at 12 months following the injury near normal trunk extension was achieved
and forward flexion enabled fingertips to reach the mid tibia. SLR was now
approximately 75° bilaterally. Subtle reduction in light touch sensation persisted over
the lateral aspect of the left leg.
Repeated MRI at 4.5 years demonstrated further reduction in the extent of the L4-5 disc
herniation since the six month assessment (Figures 9.1 & 9.2). Mild reduction in light
touch sensation persisted. Spinal mobility was slightly limited although movements
were pain free. Symptoms had reduced markedly with report of only occasional activity
related low back pain, in parallel with resumption of normal activity levels.
At the 12 year follow up the patient described minor intermittent left lumbar and
posterior thigh pain associated with sustained sitting. There had been further recent
reduction in these residual symptoms following commencement of regular walking. On
physical examination there was a good range of lumbar active movement with only
slight reproduction of left lumbosacral pain at end range extension. There were no reflex
or power changes and only slight reduction to light touch sensation over the lateral left
lower leg. Straight leg raising was unremarkable and asymptomatic at 85° bilaterally.
MRI on this occasion revealed visible minor residual disc material extending into the
spinal canal but no indentation of the thecal sac. Additionally moderate disc
degeneration was noted at L4-5 with reduction in disc height, end plate irregularity and
osteophytosis. While some degree of degenerative change was noted in 1997 this had
progressed from mild to moderate in the ensuing period.
Retrospective analysis of serial axial T2 weighted images were quantified for thecal sac
A-P dimensions and cross sectional area of multifidus using image analysis software
(NIH Image-J, Bethesda, USA) (Figure 9.3). Fat infiltration of multifidus was measured
using the same image analysis software. Histograms of pixel values were generated of a
region of interest within both muscle and subcutaneous fat from which the percentage of
fat and muscle within the multifidus region (Figure 9.3) was calculated (Table 9.1).
Chapter 9: The longitudinal case study
Page IX-6
Figure 9.3: Axial image showing method used to derive linear (A) and area (B)
measurements of thecal sac and multifidus area respectively. Histograms depict pixel
values from muscle (C) and subcutaneous fat (D) and multifidus area (E).
Table 9.1: Summary of results of thecal sac A-P measurements, multifidus cross
sectional area and fat infiltration.
Year Intervertebral
Level
Thecal
sac A-P
(mm)
Multifidus CSA (mm) Fat infiltration (%)
Right Left Right Left
1997 L3-4 14.98 871.77 867.11 39.2 33.46
L4-5 9.4 1058.1 1081.38 34.42 32.02
1998 L3-4 16.58 798.57 696.38 67.51 60.6
L4-5 15.2 922.6 900.72 76.66 53.35
2002 L3-4 16.67 713.18 659.02 37.96 40.63
L4-5 13.33 874.81 821.13 41.61 47.24
2009 L3-4 15.88 855.14 837.79 24.64 17.93
L4-5 14.8 1040.84 1001.34 20.02 26.32
9.4 Discussion
This case follows the natural history over 12 years of symptoms and MRI changes in a
case of conservatively managed HNP. Few reports in the literature span a period of this
duration. It is clear that the greatest reduction in herniation size, as represented by thecal
sac A-P dimension, occurred in the initial six month period with continued reduction
over the remainder of the observation period.
Cross sectional area of the multifidus region was reduced bilaterally at both the level of
injury and the level above. This was a steady reduction over five years following which
there was recovery to almost initial levels. Previous studies have reported that atrophy is
level and side specific and does not spontaneously recover (Hides et al., 1996; Hides et
al., 1994). The results of our case study do not support this conclusion. It may be
Chapter 9: The longitudinal case study
Page IX-7
hypothesised that the presence of bilateral lumbar symptoms or the polysegmental
nature of some fascicles of multifidus may have contributed to this variation. The
profound initial atrophy seen may in part result from modification of the patient’s
occupation and functional activities to accommodate the requirement for more
conservative spinal loading during the post-injury period. As the patient did not
undertake a formal exercise program aimed at specific muscle retraining, any changes
identified would be attributable to general activity.
Fat infiltration in the same muscle group showed an initial increase followed by a
decrease over ensuing years. Changes were bilateral and demonstrated at adjacent
levels. Fat infiltration has been postulated to result from either disuse atrophy or
denervation (Elliott et al., 2008) but no conclusive evidence exists to explain its cause.
It is noteworthy that the observed morphological change demonstrated reversal by 12
years post injury. This may be an effect of increased physical activity over the last 18
months during which the patient commenced regular walking exercise.
9.5 Conclusion
This case illustrates conservative management of HNP. Spontaneous resorption of
extruded nucleus pulposus occurs mainly in the first six months but continues gradually
over years. Changes to muscle cross sectional area and fat infiltration may occur at
several levels and may reverse even many years post injury.
Chapter 9: The longitudinal case study
Page IX-8
9.6 References
Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain. London,:
Churchill Livingstone, 2002.
Atlas SJ, Keller RB, Wu YA, Deyo RA, Singer DE. Long-term outcomes of surgical
and nonsurgical management of sciatica secondary to a lumbar disc herniation:
10 year results from the maine lumbar spine study. Spine 2005; 30(8): 927-35.
Autio RA, Karppinen J, Niinimaki J, Ojala R, Kurunlahti M, Haapea M, Vanharanta H,
Tervonen O. Determinants of spontaneous resorption of intervertebral disc
herniations. Spine 2006; 31(11): 1247-52.
Barker KL, Shamley DR, Jackson D. Changes in the cross-sectional area of multifidus
and psoas in patients with unilateral back pain: the relationship to pain and
disability. Spine 2004; 29(22): E515-9.
Benoist M. The natural history of lumbar disc herniation and radiculopathy. Joint Bone
Spine 2002; 69(2): 155-60.
Cribb GL, Jaffray DC, Cassar-Pullicino VN. Observations on the natural history of
massive lumbar disc herniation. J Bone Joint Surg Br 2007; 89(6): 782-4.
Danneels LA, Vanderstraeten GG, Cambier DC, Witvrouw EE, De Cuyper HJ. CT
imaging of trunk muscles in chronic low back pain patients and healthy control
subjects. Eur Spine J 2000; 9(4): 266-72.
Elliott J, Sterling M, Noteboom JT, Darnell R, Galloway G, Jull G. Fatty infiltrate in the
cervical extensor muscles is not a feature of chronic, insidious-onset neck pain.
Clin Radiol 2008; 63(6): 681-7.
Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsion on
the lumbar intervertebral joints: the role of torsion in the production of disc
degeneration. J Bone Joint Surg Am 1970; 52(3): 468-97.
Hides JA, Gilmorea C, Stanton W, Bohlscheida E. Multifidus size and symmetry among
chronic LBP and healthy asymptomatic subjects. Manual Therapy 2008; 13: 43-
9.
Hides JA, Richardson CA, Jull GA. Multifidus muscle recovery is not automatic after
resolution of acute, first-episode low back pain. Spine 1996; 21(23): 2763-9.
Hides JA, Stokes MJ, Saide M, Jull GA, Cooper DH. Evidence of lumbar multifidus
muscle wasting ipsilateral to symptoms in patients with acute/subacute low back
pain. Spine 1994; 19(2): 165-72.
Kim MS, Park KW, Hwang C, Lee YK, Koo KH, Chang BS, Lee CK, Lee DH.
Recurrence rate of lumbar disc herniation after open discectomy in active young
men. Spine 2009; 34(1): 24-9.
Kjaer P, Bendix T, Sorensen JS, Korsholm L, Leboeuf-Yde C. Are MRI-defined fat
infiltrations in the multifidus muscles associated with low back pain? BMC Med
2007; 5: 2.
Kobayashi N, Asamoto S, Doi H, Ikeda Y, Matusmoto K. Spontaneous regression of
herniated cervical disc. Spine J 2003; 3(2): 171-3.
Mengiardi B, Schmid MR, Boos N, Pfirrmann CW, Brunner F, Elfering A, Hodler J. Fat
content of lumbar paraspinal muscles in patients with chronic low back pain and
in asymptomatic volunteers: quantification with MR spectroscopy. Radiology
2006; 240(3): 786-92.
Scannell JP, McGill SM. Disc prolapse: evidence of reversal with repeated extension.
Spine 2009; 34(4): 344-50.
Singer KP, Fazey PJ. Disc herniation - non operative treatment. In: Herkowitiz HK,
Dvorak J, Bell G, Nordin M, Grob D editors, The Lumbar Spine, Philadelphia:
Lippincott Williams and Wilkins, 2004.
CHAPTER 10
Page X-1
Discussion
10.1 Introduction
Over the last century the focus in the spine literature concerning functional mechanics
has been primarily on sagittal plane and less on coronal and axial plane motion. The
purpose of this thesis was to elaborate the functional and mechanical significance of
rotation as it relates to NP deformation.
Several questions naturally arise from this; what is normal, what is abnormal? What is
the effect of age, deformity or injury? Can NP deformation be used to predict the degree
of deformity in scoliosis? Arising from these questions are several themes which will be
expanded in this chapter.
1. Fundamental normal mechanics of NP deformation relative to position.
2. The effect of age and deformity on NP deformation magnitude and predictability
of direction.
3. Differences between the normal and the abnormal.
10.2 Thesis evolution
Chapter 4 of this thesis investigated the effect on rotation range of common
morphological variations involving both facet joints and the IVD. An increase in
available intersegmental range of axial rotation was reported in the presence of IVD
degeneration. This result was consistent with other reports in the literature (Haughton et
al., 2002; Johansen et al., 1999; Singer et al., 2001). As the degenerative process
involves reduction in proteoglycan and therefore water content in the IVD, particularly
the NP, the converse question was raised; what is the mechanical effect of axial rotation
on the hydrostatic mechanism of the lumbar NP?
Appendix 4 documents and approach to examine this question using a novel pixel
profiling method and T2 weighted MRI sequences in young normal subjects. While a
directional bias in NP deformation was seen, the small number of subjects dictated that
a larger cohort be examined with this method and consequently this is reported in
chapter 5.
Chapter 10: Discussion
Page X-2
As early results indicated limited predictability of NP deformation in response to axial
rotation position it was hypothesised that conjunct coronal plane motion may have a
more predictable influence. This is postulated in Appendix 4 and chapter 5, and tested
in chapter 6 with application of a refined method to a cohort of young normal subjects
positioned in lumbar lateral flexion.
The natural progression from normal subjects was to extend the method and hypothesis
to age related and spinal deformity cases. Chapter 7 repeats the protocol examining NP
deformation following axial rotation in an older population, some of whom exhibited
age-related degenerative IVD change. Chapter 8 focuses on subjects with idiopathic
scoliosis, a structural pathology involving deformity in both axial and coronal planes.
Rotary injury to the IVD is common and may result in interruption to the internal IVD
environment. Chapter 9 examines this via detailed analysis of a single case of IVD
herniation over 12 years, and also extends to consider concomitant perispinal tissue
effects of chronic pain and disuse atrophy. A single case study reporting rotational
injury and fracture patterns in the presence of skeletal pathology is presented in
Appendix 10.
The effect of axial rotation on predictability of NP deformation has not previously been
reported. Such an examination of the question through the progression described above
contributes an original insight to the literature.
10.2.1 Terminology
Earlier studies, and those of Appendix 4, use the term ‘migration’ when describing
observed changes in NP signal. While there have been reported assessments of this
linear change relative to AF boundaries using a variety of methods (Alexander et al.,
2007; Beattie et al., 1994; Fennell et al., 1996) conclusions cannot be drawn as to
changes in fluid distribution within the NP from such an assessment. Intact inner anular
fibres will constrain NP migration thereby limiting the value of assessments of
magnitude (Figure 10.1). These observations lead to a change in terminology from
chapter 5 to NP ‘deformation’ which was considered more conceptually accurate and
indicative of the variables being tested.
Chapter 10: Discussion
Page X-3
Figure 10.1: Schematic representation to propose that intact inner anular fibres limit migration of NP boundaries but allow internal hydration redistribution to attenuate load. (Adapted from Kramer, 1981).
10.3 Theme one – what is normal?
There is an extensive literature reporting normal reference ranges for lumbar motion in
the three cardinal planes (White & Panjabi, 1990). Less information is available for
lateral flexion and axial rotation of the lumbar segments; the main emphasis has been
due to the relative simplicity of measurement of sagittal ranges. The advent of cross
sectional imaging and multiplanar formatting has enabled more detailed insights into
other planar motion and indeed coupled motion. This section details the main insights
made with respect to the derived data from MRI sequences performed using different
cohorts of subjects.
10.3.1 Rotation range
Normal lumbar segmental rotation ranges measured with a variety of methods are
reported in the literature and discussed in chapter 2. Chapter 6 reports rotation ranges in
young asymptomatic subjects but only as a secondary response to primary positioning
into lateral flexion. Consequently they are smaller in magnitude than in reports where
axial rotation is the primary focus either in vivo or ex vivo.
10.3.2 Lateral flexion range
Chapter 6 focuses on lumbar lateral flexion in normal subjects and reports
intersegmental angles. These are greater at the apex, typically L2-3 or L3-4, and least at
the junctional zones. These ranges are smaller than those reported in the literature
(Pearcy & Tibrewal, 1984) possibly reflecting the difference between imaging
modalities or supine versus erect subject positioning.
Chapter 10: Discussion
Page X-4
10.3.3 NP deformation
The studies reported in Appendix 4 and chapter 5 quantify lumbar NP deformation
following axial rotation positioning. Chapter 6 does so following lumbar lateral flexion
positioning. In the absence of pre-existing data in the literature, these studies establish
preliminary normal values with respect to magnitude and direction.
10.3.3.1 Direction of NP deformation
The hydrostatic nature of NP mechanics is well established. The hydrated NP will
deform away from compressive load (Keyes & Compere, 1932). The direction of
deformation may then indicate the impact of net compressive load direction. In complex
spinal motion that involves multiplanar coincident motion (White & Panjabi, 1990) it
would be reasonable to infer that the greater load vector will dictate the overall direction
of NP deformation.
Strong directional bias has been reported in sagittal plane positioning in Appendix 4,
this was also found in coronal plane positioning as reported in the lateral flexion cohort
MRI study (chapter 6). This trend is consistent with the literature on this topic in the
sagittal plane (Beattie et al., 1994; Brault et al., 1997; Edmondston et al., 2000; Fennell
et al., 1996). No data exists for coronal plane positioning.
However, there were several isolated cases where deformation direction was opposite in
normal discs and this has also been reported in the literature. A possible mechanism for
this finding may be that tensile forces in the inner anulus unilaterally exceed
compressive forces on the opposite side. The net force will then be directed towards the
compressive load rather than away. However, such an hypothesis has not been tested. In
general NP deformation is highly predictable in the sagittal and coronal planes.
Far less predictability of NP deformation direction was seen subsequent to axial rotation
in young normal subjects. The effect on predictability of NP deformation with the
addition of the variables flexion or extension co-positioning was examined in a small
group, and reported in the pilot study (Appendix 4). The unpredictability of NP
deformation was was shown in a larger group in the normative cohort MRI study
(chapter 5) where it was reported that 56% of NPs deformed contralateral to the
direction of rotation and 44% ipsilaterally. However this latter study demonstrated that
75% of NPs deformed contralaterally to the direction of conjunct lateral flexion, thereby
prompting the lateral flexion cohort MRI study (chapter 6). Additionally it was seen that
Chapter 10: Discussion
Page X-5
95% deformed inversely in response to sagittal plane positioning. The general trends for
NP deformation direction relative to positioning are depicted in Figure 10.2.
Figure 10.2: Direction of NP deformation following coronal (lateral flexion) axial (rotation) and sagittal (flexion) positioning.
A reasonable conclusion from these results is that the predictability of direction of
deformation relates to available intersegmental range of motion in any given direction.
Axial rotation (with the smallest range of motion) is least predictable (approximately
50%) while coronal (95%) and sagittal (95%) planes clearly show stronger
predictability associated with greater ranges of motion.
10.3.3.2 Magnitude of NP deformation
The magnitude of NP deformation was reported as a mean percentage.
Using the peak pixel tracking method the pilot study (Appendix 4) showed a 19%
lateral deformation of the NP when subjects were positioned in rotation plus extension
and 9% when positioned in rotation plus flexion. These figures are greater than those of
Chapter 10: Discussion
Page X-6
the normative cohort MRI study (chapter 5) which reported a mean of 5.5%. Both these
studies positioned subjects in flexion and extension therefore differences cannot be
ascribed to positioning. The variation in the pilot study (Appendix 4) differs from the
literature which reports greater segmental rotation in flexion and less in extension
(Burnett et al., 2008; Pearcy et al., 1984; Pearcy & Tibrewal, 1984; Pearcy, 1993;
Pearcy & Hindle, 1991).
Deformation magnitude in the lateral flexion cohort study (chapter 6) averaged 16.4%.
This was greater at the apex of the curve and less at the superior and inferior regional
limits. Greater subject numbers, plus the inclusion of all lumbar segments in this study
enabled a more thorough analysis. The magnitude was generally greater than that seen
in the rotation studies, though less than that seen in the pilot study (Appendix 4) where
sagittal plane data was assessed.
It would be reasonable to conclude from these results that the predictability of NP
deformation direction is relative to the magnitude of available intersegmental range in
any cardinal plane. However, the magnitude of NP deformation was found not to be
proportional to the magnitude of intersegmental range.
10.4 Theme two – what is the effect of age and deformity?
The second series of studies including the older cohort MRI study (chapter 7), the
scoliosis cohort MRI study (chapter 8) and the longitudinal case study (chapter 9)
applies the previously developed method to cohorts with degnerative IVD changes plus
those with a primary spinal deformity. While it can be argued that degenerative change
is consequential to normal ageing rather than a pathology, it is included here to
complement observations drawn from the young normal population.
10.4.1 Ageing discs
The older cohort MRI study (chapter 7) reports a study of subjects aged between 40 and
57, years with variable degenerative change in some or all lumbar discs. Few studies
have investigated changes to NP signal in sagittal plane positions and none have
investigated rotation effects. Reference was made to differences in aged discs in only
one related study (Edmondston et al., 2000), concluding that directional bias was less
predictable in older discs. This is the first such study to report NP deformation specific
to rotation in graded degenerated discs.
Chapter 10: Discussion
Page X-7
NP deformation is fundamentally governed by hydrodynamic principles. Degenerative
change within the IVD primarily results in loss of fluid, reduction in disc height and
subsequent modification of load bearing (see chapter 2, section 2.2). Other mechanical
changes result, including increased intersegmental range of rotation as reported in
chapter 4. The interrelationship of these changes raises the question as to the effect of
IVD degeneration on NP deformation resulting from axial rotation and how this might
differ from the normal.
Using the same image analysis protocol described in the normative and lateral flexion
cohort MRI studies (chapters 5 and 6), the older cohort MRI study (chapter 7) showed a
mean coronal NP deformation of 2.3%, less than half the normative data reported in
chapter 5. The magnitude of change in the NP deformation was therefore most evident
in the younger cohorts where the NP signal could be clearly seen offset from the
compression load axis. In contrast, the older cohort showed NPs with lower signal and
for whom the NP deformation was both less evident and smaller in magnitude.
Consequently, the results for the older cohorts challenge the utility of the current
method given that the measurement error is slightly greater than the mean change
recorded for those discs with correspondingly more pronounced degenerative changes.
A trend towards deformation being greater at L1-2 may be explained by fewer cases
with degenerative change in the upper lumbar levels.
In the older cohort, directional bias was similar to the normative (younger) cohort, with
approximately half of the NPs deforming towards the left (47.3%) and half right
(52.7%). When this was compared with the direction of segmental lateral flexion it was
seen that 61.8% deformed to the contralateral side. This is less than the 75% reported in
the normative cohort MRI study (chapter 5). Gender bias in direction is noted and
unexplained, possibly reflecting the small number of cases.
On the basis of these results it would be reasonable to dispute the propositions in the
literature that NP deformation direction is less predictable in discs with degenerative
change (Edmondston et al., 2000; Modic & Ross, 2007). Caution should be exercised as
these two studies employ an alternative method, using T2 weighted MR images and a
pixel intensity method applied to sagittal images, with only a single line transect across
the mid disc region.
Chapter 10: Discussion
Page X-8
Comparison between results in the normative and older cohort MRI studies (chapters 5
and 7) also warrants circumspection, in recognition of the method variable of sagittal
plane positioning which was used only in the normative cohort study (chapter 5).
While it is stated that water loss in the IVD reduces hydrostatic properties evidence is
not forthcoming to support this (Modic & Ross, 2007). The study in chapter 7 disputes
this claim as predictability is unaffected; only the magnitude of the hydrostatic effect is
reduced.
As the IVD loses water content the T2 weighted MRI signal reduces and reveals a
patchy hydration pattern (Figure 10.3). Areas of retained hydration will likely continue
to behave hydrostatically but the inconsistent distribution would reduce the overall
effect. Claims of reduced predictability may be an effect of single line samples being
less representative of the whole IVD.
Degenerative change is often accompanied by formation of clefts between concentric
anular rings. This may allow extrusion of NP material into these clefts, further
redistributing NP and rendering hydration difficult to ascertain from single line pixel
samples in the sagittal plane. Multiple line samples, as used in chapter 7, particularly
from axial images, have a greater likelihood of capturing signal from NP infiltration of
anular clefts and therefore inclusion in any quantification of NP deformation.
24 year old male 48 year old male
Figure 10.3: Three dimensional surface plot profile of pixel intensity signal from T2
weighted axial MRI showing normal hydration patterns (A) with clearly increased signal from NP and (B) patchy hydration and markedly reduced signal intensity from
the NP of a degenerate disc. As the NP loses hydrostatic pressure its load attenuation ability is compromised while
the AF takes more load (Figure 10.4). This reversal of proportional load bearing may
also contribute to reduced NP deformation as pressure from the AF and associated
A B
Chapter 10: Discussion
Page X-9
inward buckling of the inner anular fibres (Meakin et al., 2001) (Figure 10.5) may
further constrain the NP generally.
Figure 10.4: Loss of NP fluid content in degenerative disc disease (DDD) leading to increased loading of AF may contribute to reduced NP deformation magnitude.
Figure 10.5: Inward buckling of inner anular fibres (arrow) may constrain NP
deformation. (Adapted from Adams, 2002)
Nucleus pulposus deformation in response to axial rotation has therefore been shown to
be less predictable than positioning in the sagittal and coronal planes but similarly
predictable between younger and older subjects.
10.4.2 Scoliosis
Scoliosis is the only multiplanar structural deformity that typically includes changes in
both coronal and axial planes. Since these are the two primary planes considered as
variables in this thesis, scoliosis provides an ideal clinical model from which to examine
the effect of a long standing multiplanar structural deviation on IVD deformation.
Chapter 10: Discussion
Page X-10
The mechanics of scoliosis and the presenting deformity are described in the scoliosis
cohort MRI study (chapter 8).
10.4.2.1 Range of lateral flexion in scoliosis
Chapter 8 reports data obtained from the intervertebral level at the apex of secondary
lumbar scoliotic curves. Most often the peak of the lumbar curve occurred at L2-3
(50%) followed by T12-L1 (28%) and the mean intersegmental lateral flexion angle was
7.5°. In the normal subjects reported in the lateral flexion cohort MRI study (chapter 6)
the most common lumbar lateral flexion apex was L3-4 and the range of intersegmental
lateral flexion at each segment averaged 6.1°.
This relatively small difference in mean ranges may result from segmental level
variations or the effect of averaging over all lumbar segments. Additionally, the subjects
in the lateral flexion cohort MRI study (chapter 6) were placed and constrained into end
range lateral flexion while those in the scoliosis cohort MRI study (chapter 8) were
positioned without imposed postural constraint and therefore not necessarily at the end
range of segmental lateral flexion.
While much data exists on the degree of curvature of the scoliotic spine it describes
predominantly the primary thoracic curve as measured by the method described by
Cobb, rather than measurements of specific intersegmental angles. Few comparative
data exist for segmental ranges in secondary lumbar scoliotic curves.
10.4.2.2 Range of rotation in scoliosis
The direction of segmental rotation in the scoliosis cohort MRI study (chapter 8) was
ipsilateral to the coronal deformity in all cases. This is a function of the complex and
poorly understood etiology of scoliosis (Kouwenhoven & Castelein, 2008).
Mean segmental rotation between the vertebral bodies adjacent to the apical IVD was
4.6°. In contrast, the lateral flexion cohort MRI study (chapter 6) reports much smaller
ranges, however rotation was only coincident as primary positioning was into lateral
flexion. Comparison is therefore limited. Additionally, rotation in scoliosis occurs not
only at the IVD level but within the bodies of the vertebrae (Birchall et al., 2005) so
cannot accurately be termed intersegmental. Few comparative data exist for segmental
rotation angles in secondary lumbar curves of scoliotic spines.
Chapter 10: Discussion
Page X-11
10.4.2.3 NP deformation
Mean coronal plane NP deformation in scoliotic spines was 12.9% while that of normal
subjects was 11.3%. This small difference may be a function of data being derived from
apical segments rather than averaged from all lumbar levels. In each scoliotic case the
deformation direction was towards the convexity. In contrast, in 4/105 of the discs in
normal laterally flexed subjects (chapter 6) the deformation was away from the
convexity.
There was no association between NP deformation magnitude and degree of segmental
lateral flexion in the scoliotic curves, however a moderate association existed in the non
scoliotic spines reported in the lateral flexion cohort MRI study (chapter 6). This
association needs to be tested with greater subject numbers for a more thorough
comparison. It is hypothesised that at best a poor association occurs at extremes of
range, where the creep effect allows further increase in lateral flexion range but the
tensile force in intact inner anular fibres prevents further NP deformation. This could be
tested by gathering data on NP deformation at selected sub maximal ranges of lateral
flexion.
Scoliosis is a rare topic area in which IVD hydration has been discussed in the
literature. A method of three dimensional mathematical modelling of the NP in scoliosis
has been developed and reported (Périé et al., 2001). This was later used to characterise
NP migration in response to mechanical effects but only in coronal and sagittal planes
(Périé et al., 2003). Migration to the convexity was reported in all cases and was
consistent with chapter 8 conclusions.
A similar method was validated and used by Violas pre and post operatively in scoliosis
to examine the effect on non stabilised lumbar discs (Violas et al., 2007a, b; Violas et
al., 2005). Quantification of both NP and whole disc volume was reported, without
consideration of variations of hydration pattern within the IVD or specific reference to
axial plane movement changes or influence on such patterns.
The scoliosis cohort MRI study (chapter 8) takes this concept further, not only
supplying directional data but also mapping of hydration patterns within the NP.
Additionally, axial plane influence on hydration patterns is considered where other
investigators have not. The chapter 8 study does not attempt to quantify total disc
hydration.
Chapter 10: Discussion
Page X-12
In general scoliotic motion segments analysed in chapter 8 showed a more consistent
NP deformation directional bias than those of non scoliotic spines in chapters 4-7. As
rotation and lateral flexion components of the deformity always occur in tandem it is
not possible to separate the effect of coronal and axial plane positioning. The preceding
studies suggested that lateral flexion direction more strongly predicts deformation
direction. However, clarification of this question may not be assisted by examining
scoliotic spines, given the triplanar nature of that pathology.
10.4.3 IVD herniation
IVD herniation is a common injury frequently caused by rotation strains (Scannell &
McGill, 2009) and the most frequently occurring primary pathology involving extrusion
of NP material (Moore et al., 1996). The effect is to disrupt the internal homeostasis of
the disc, thereby potentially altering its mechanical properties and ability to attenuate
load. Figure 10.4 represents the mechanism by which altered load bearing results from
loss of NP hydration over time. Herniated NP also effectively reduces the hydration
volume as some NP material escapes the disc interior. This may contribute to
accelerated onset of degeneration (Farfan et al., 1970). Even minor disruption of the AF
during discography has been shown to contribute to early degenerative change
(Carragee et al., 2004).
The longitudinal case study (chapter 9) considers this primary rotational and NP-related
pathology and reports a unique longitudinal case study of variables other than NP
deformation. These include tracking cross sectional area of lumbar multifidus and the
thecal sac, in addition to fat infiltration of multifidus over a 12 year period. The findings
are compared with the relevant literature. While these parameters have been previously
reported for both the cervical (Elliott et al., 2008) and lumbar (Hides et al., 2008)
regions, they have not been tested over such an extended timeframe subsequent to
lumbar rotational injury and NP changes due to loss of intradiscal structural integrity.
The protracted duration of this longitudinal study permits reporting of late changes in
muscle cross sectional area and fat infiltration, and the prospect for restoration with
exercise after long established injury.
Chapter 10: Discussion
Page X-13
10.4.3.1 NP deformation
The deformation of the NP following AF disruption is macroscopically evident. In the
reported longitudinal case study (chapter 9), the direction was central into the spinal
canal where it tracked superiorly along the theca. This was measured and changes
followed in thecal sac A-P dimension. Clearly NP deformation was markedly greater
than the previous studies in Appendix 4 and chapter 5 which included flexion
positioning as these subjects retained intact anuli.
Directional bias depends upon the location of AF disruption. Predisposition to certain
locations for AF disruption may be pre-existent and associated with underlying anular
tears which may lead to the formation of clefts (Osti et al., 1990). As flexion has been
shown to deform the NP posteriorly in the majority of cases the occurrence of NP
herniation in the posterior half of the disc is unsurprising. The rotational component of
the injuring mechanism would in theory have a different effect. It has been shown that
increasing intersegmental rotation causes the axis of motion to migrate towards the
compression facet (Wachowski et al., 2009). This would result in the greatest force
being directed at the point most distant from the axis – in this case the anterolateral
anulus. If rotation was the dominant causative factor then herniations would occur in
that region. The predilection of herniations for the posterior anulus suggests that flexion
is more dominant in causation. The anatomical variation in AF depth between anterior
and posterior is also a contributing factor.
Further direct comparison with previous studies in chapters 5-8 beyond the sagittal
plane is invalid as positioning for MRI was neutral with no coronal or axial component.
10.4.3.2 Fat infiltration and cross sectional area
Fat infiltration and cross sectional area (CSA) of multifidus are reported in the
longitudinal case study (chapter 9) and vary somewhat from previous reports in the
literature. Reduction in cross sectional area is reported to be specific to the side of
symptoms and the intervertebral level involved (Hides et al., 1994). Chapter 9 also
reports a reduction in cross sectional area but it is neither isolated to the intervertebral
level of herniation nor the side of symptoms. Multifidus contains both long and short
fascicles, the latter crossing several segments between bony attachments (Rosatelli et
al., 2008). A cross sectional sample at a given level will therefore capture both, however
not all necessarily have direct connection to that level. It could therefore be expected
Chapter 10: Discussion
Page X-14
that atrophy would be evident at other levels within the region (as reported in the
longitudinal case study in chapter 9) which also shows changes bilaterally.
The literature reports a reduction in Multifidus CSA post injury but proposes that this
does not reverse spontaneously unless very specific exercises are undertaken (Hides et
al., 1996). Chapter 9 results do not support this theory as an increase in CSA was seen
12 years post injury without intervention beyond an increase in normal activity level
over time.
Fat infiltration followed a similar trend, with an initial increase post injury and
reduction at 12 years raising the possibility of association with CSA.
10.5 Limitations
Identification of study limitations are important to avoid over interpretation and
inappropriate extrapolation. The limitations relevant generally across the study series
will be elaborated.
10.5.1 Samples
Convenience samples were used in each of the cohort studies to generate and test
hypotheses. It is not intended that the sample sizes were adequate for full statistical
analysis, rather to describe and report preliminary trends. Recommendations for future
studies (chapter 11) addresses several areas where larger samples of more homogeneous
cohorts (age, disease, deformity) could be assessed.
10.5.2 Magnetic Resonance Imaging
All MRI studies were undertaken in a conventional closed magnet. This limited subject
selection to those of a body size and shape amenable to positioning within the confines
of the magnet bore. Subject selection was also limited by general contraindications to
MRI as defined in Appendix 3. The conventional nature of the magnet requires non-
weighbearing positioning of subjects limiting functional relevance of results.
Evolution of novel method changes over a 7 year study period, incorporating a change
in MRI unit from a 1 Tesla to a 1.5 Tesla model, meant no retrospective pooling and
comparisons were possible. However, general trends were noted across cohort studies.
During the course of the various studies four different MRI technologists provided
support during scheduled weekend research blocks. Subtle differences in approaches to
acquisition of the different sequences, despite written protocols, may have meant the
Chapter 10: Discussion
Page X-15
image data were not entirely consistent. This is especially so for determining coronal
slice position used to define lateral flexion angles.
10.5.3 Data comparison
Data derived from each cohort reflected mixed gender and age samples which
contributed to the variability within these data sets.
10.6 Clinical implications
The results from these studies reveal NP deformation direction to be highly predictable
in the sagittal and coronal plane but not in the axial plane. Magnitude of NP
deformation and range of segmental movement are not strongly associated.
There are several practical implications of this new knowledge.
A commonly used intervention for management of low back pain is predicated on the
presumption that discogenic pain results from NP deformation against a damaged and
pain sensitive anulus (McKenzie & May, 2003). Passive and active movements and
postures in sagittal, coronal and axial planes are employed on this basis to impart a
predictable mechanical effect on the NP position. MRI studies of NP deformation will
provide the basis for a better understanding of these interventions and their mechanical
effects.
Postural scoliosis in acute low back pain is common and associated with lumbar disc
injury and sciatica (Akhaddar et al., 2011). Advanced knowledge of IVD and NP
mechanics will elaborate the potential mutability of the NP to corrective mechanical
forces in internal disc disruption. Limited case based evidence exists for this concept
and it association with symptom reduction (Appendix 5).
Torsional anular injury may result in frank NP herniation. Better understanding of the
mechanical effect of primary plane movement and position through such MRI based
studies may help inform conservative management protocols.
Better understanding of lumbar NP behaviour relative to positioning will potentially
assist in further development of artificial discs.
Chapter 10: Discussion
Page X-16
Perianular ossification related to loss of rotation control has been reported (Fraser et al.,
2004). This may be avoided with expanded knowledge of the mechanical effects of
rotation on the NP.
NP replacement is also becoming more frequent and its refinement will benefit from
such knowledge (Coric & Mummaneni, 2008; Puentedura et al., 2010). Replication of
the complex biomechanical properties of the motion segment using such biodevices is
challenging and requires detailed knowledge of normal mechanics (Costi et al., 2011).
Knowledge of NP deformation patterns may also inform the study of ergonomics from a
better understanding of biomechanics to minimise posterior anular wall strain relative to
lumbar position.
Chapter 10: Discussion
Page X-17
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CHAPTER 11
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Conclusions and recommendations
The primary purpose of this thesis investigation was to quantify the in vivo effect of
rotation postures on lumbar NP deformation and to report the predictability of the
direction of that deformation. Additionally, the effects of coincident coronal plane
positions, age related changes and spinal deformity (scoliosis) were examined to
determine the relative influences of such factors on the internal mechanism of the IVD.
The principal hypothesis was that the NP would deform in all cases and conditions in a
predictable direction and with a magnitude proportional to the resultant segmental
angulation.
Secondary hypotheses, tested in the individual investigations that form the complete
series, are addressed below.
The primary method for measuring NP deformation magnitude was shown to be
reliable.
11.1 The ex vivo CT study (chapter 4)
The objective of this study was to examine the influence of lumbar zygapophysial joint
anatomy and intervertebral disc pathology on axial torsion response in ex-vivo
ligamentous lumbar spine preparations using 3D motion tracking and computed
tomography (CT). This study concluded that:
1. Axial rotation and joint separation was greatest for the lower lumbar segments
which corresponded with larger coronal joint angles.
2. Semi-flexion generally resulted in increased segmental rotation compared with
neutral and extension positions, except in the presence of marked segmental
degeneration.
3. Separation of the zygapophysial joint is a normal response during axial rotation
movements. However, anatomical configuration of the paired zygapophysial
joints, and the stage of degenerative disc disease impacts on segmental mobility.
This study generated the hypotheses which informed the following studies.
Chapter 11: Conclusions and recommendations
Page XI-2
11.2 The pilot study (appendix 1)
The aim of this study was to assess a novel method using MRI to track NP deformation
following positioning into flexion and extension, and the combined positions of flexion
plus left rotation and extension plus left rotation in the lumbar spine, at L1-2 and L4-5.
This study concluded that:
1. The method was reliable.
2. That a predictable pattern of anterior NP deformation was evident following a
change in sagittal plane position from one of flexion to extension in the target
intervertebral discs.
3. There was a trend to NP deformation to the right with the addition of left
rotation positioning.
11.3 The normative cohort MRI study (chapter 5)
This study was designed to test the hypothesis that NP deformation subsequent to
sagittal, axial and conjunct coronal plane positioning would demonstrate predictable
directionality. Results showed that NP deformation direction was highly predictable
following sagittal plane position change as 19/20 cases deformed towards the convexity.
Axial plane positioning into left rotation showed 44% of NPs deformed to the left and
56% deformed to the right. In 75% of cases the NP deformed to the opposite side to
coincident intersegmental lateral flexion.
The following conclusions were therefore drawn:
1. The hypothesis was accepted with respect to sagittal plane positions as results
demonstrated that the direction of NP deformation after lumbar sagittal plane
positional change was predictable.
2. Deformation of the NP following adoption of rotated positions in flexion and
extension was reduced in magnitude and less predictable with respect to
direction.
3. That the direction of coincident intersegmental lateral flexion was a stronger
predictor of NP deformation direction than axial rotation direction.
11.4 The lateral flexion cohort MRI study (chapter 6)
This study sought to assess the effect of coronal plane positioning alone on NP
deformation. This tested the hypothesis that the NP would deform predictably towards
Chapter 11: Conclusions and recommendations
Page XI-3
the convexity and with a magnitude proportional to the range of segmental lateral
flexion. Reported results were:
1. That the NP displaced away from the direction of lateral flexion in 95/105 discs
(P<0.001).
2. That the extent of NP displacement was associated strongly with lateral flexion
at L2-3 (P<0.01).
3. The greatest range of lateral flexion occurred at L2-3, L3-4 and L4-5. Small
intersegmental ranges of axial rotation occurred at all levels but were not
associated with NP displacement.
From these results the following conclusions were drawn:
1. Direction of NP deformation was highly predictable in laterally flexed healthy
lumbar spines.
2. The magnitude of displacement was not commensurate with the degree of
intersegmental lateral flexion or rotation.
Consequently the hypothesis that magnitude would be proportional to the degree of
lateral flexion was rejected and the hypothesis that NP deformation would be towards
the convexity was accepted.
11.5 The older cohort MRI study (chapter 7)
The purpose of this study was to test the influence of age related changes on NP
deformation and therefore to test the hypotheses that greater segment lateral flexion and
rotation would induce the largest NP deformation from the neutral position; that more
severe disc degeneration would reduce the extent of any NP deformation and that the
NP would deform contralaterally to the direction of segmental lateral flexion.
Mean NP deformation was 2.1% of disc width. At L3-4 there was a modest association
between lateral flexion and NP deformation (r=0.38, p<0.034). In the left rotation
position 47.3% of all discs deformed to the left and 52.7% to the right; 61.8% deformed
contralateral to the direction of intersegmental lateral flexion. The following
conclusions are therefore drawn:
1. NP deformation magnitude was independent of level, grade of degeneration or
segmental lateral flexion or rotation angle.
2. The direction of NP deformation was unpredictable in rotation and poorly
predictable with respect to lateral flexion direction.
Chapter 11: Conclusions and recommendations
Page XI-4
3. The degree of degeneration did not appear to be associated with predicting the
deformation direction.
Consequently the hypotheses concerning rotation and the influence of stages of
degeneration were rejected. The hypothesis that NP deformation would occur
contralateral to the direction of segmental lateral flexion was accepted.
11.6 The scoliosis cohort MRI study (chapter 8)
This retrospective observational cohort study was undertaken to test the hypothesis that
in lumbar compensatory scoliotic curves, NP deformation magnitude at the apex of the
curve would be associated with the extent of intersegmental lateral flexion range.
Lumbar Cobb angles ranged from 12.4° to 54.6°, with a mean of 34.9°. Intersegmental
rotation at the apex ranged from 0.8° to 8.0°, with a mean of 4.6°. Segmental lateral
flexion ranged from 4.2° to 13.7°, with a mean of 7.5°. The apical NP showed an offset
away from the midline which was not associated with the extent of the Cobb angle
(r=0.12).
Adolescent lumbar compensatory scoliosis results in exaggeration of the three cardinal
planes which coupled with disc wedging contribute to an offset deformation of the NP
away from the compressive axis. While in general, the greater the disc wedging and
lumbar Cobb angles the further the displacement of the NP, there was no association
between magnitude of NP deformation and extent of Cobb angle. The hypothesis was
therefore rejected.
11.7 The longitudinal case study (chapter 9)
This 12 year retrospective longitudinal single case study followed the natural history of
a rotation injury to the IVD resulting in a large central L4-5 disc herniation. It assessed
variables including herniation size and the effect on paravertebral muscle cross sectional
area and degree of fat infiltration. It tested the hypothesis that changes in paravertabral
muscle size and composition occur with normal activity after 12 years. Changes in cross
sectional area and fat infiltration demonstrated restoration over the course of the study.
The hypothesis was therefore accepted.
Chapter 11: Conclusions and recommendations
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11.8 Recommendations for future studies
The series of studies presented in this thesis were designed to test the hypotheses as
described. Investigation of these raised further questions which could be tested in the
following proposed studies:
11.8.1 Larger cohort, three dimensional weightbearing study
A future study employing the refined method described in chapter 7 applied to a larger
cohort of subjects would be of interest. This would allow age and gender matched
analysis of results to examine for statistically significant differences. This could also
include the addition of subject positioning into both left and right rotation to test for
intra subject laterality difference in NP deformation. Ideally image acquisition would
occur within an open MRI permitting physiological loading. This would require rapid
image sequencing but would also allow a greater variety of positions to be examined,
with consideration of the functional implications of derived data.
Three dimensional image analysis may better quantify fluid shift within the confines of
the anulus and more accurately characterize directional predictability.
11.8.2 Ex vivo islolated segmental rotation study
The aim of this study would be to examine the effect of isolated intersegmental rotation
on NP deformation direction and magnitude. In vivo coupling of motion in axial and
coronal planes makes difficult the analysis of the effect of positional change in each
separately.
A torsion rig similar to that used in the ex vivo study described in chapter 4 would be
constructed with non ferrous material. Into this would be fixed a cadaveric lumbar spine
section comprising cojacent vertebral bodies and the intervening intervertebral disc with
all muscular and ligamentous attachments removed. Through an external pulley system
attached to the vertebral bodies, predetermined incremental loads would be applied to
induce isolated positional change in the cardinal planes.
The rig would be placed in an MRI scanner and a protocol employed to acquire axial,
coronal and sagittal T1 and T2 weighted images.
Image analysis in three dimensions would characterise and quantify direction of NP
deformation relative to each position and load. From this data the contribution of each
component of composite in vivo motion may be better understood.
Chapter 11: Conclusions and recommendations
Page XI-6
Preferably human material would be tested but in its absence a suitable animal surrogate
such as sheep lumbar segments could substitute (Wilke et al., 1997). Morphological and
therefore biomechanical differences between the human spine designed for bipedal
locomotion and that of a quadruped would require consideration.
11.8.3 Clinical studies
11.8.3.1 Diagnosis of discogenic pain
The primary tissue source of pain in localized, non specific low back pain cannot be
accurately determined clinically especially with reference to discogenic pain (Adams et
al., 2002). Centralisation and peripheralisation of pain correlates with proven discogenic
pain (Donelson et al., 1997) but is not considered to be diagnostic (Bogduk & Lord,
1997).
While it is accepted that low back pain is a multi structure problem, an ability to
clinically differentiate the relative contribution of disc and zygapophysial joints would
improve treatment specificity and accurately direct further investigation.
The studies described in this thesis identify greater predictability of NP deformation in
sagittal and coronal plane positioning. Most functional activities require concurrent
motion through several planes. Clinical movement examination should therefore extend
beyond the cardinal planes to combinations (Barrett et al., 1999; Edwards, 1992).
In light of reported results, clinical examination of combinations founded on sagittal and
coronal planes may ensure better predictability and understanding of the NP response.
Patterns of symptom response may elucidate potential tissue sources of pain. The
potential for combined movement to identify structural or tissue source has been
postulated (Singer et al., 2004).
Subjects with non specific low back pain would be examined with combined sagittal
and coronal plane movements using three dimensional motion analysis (Figure 11.1).
Pain and movement maps will be derived from this assessment (Barrett et al., 1999).
Results will be correlated with reproduction of concordant pain on discography or
amelioration of symptoms on zygapophysial joint block to identify primary pain source.
Chapter 11: Conclusions and recommendations
Page XI-7
Such a study as described may contribute new knowledge to clinical diagnosis and
management of low back pain.
Figure 11.1: Three dimensional motion analysis has been shown to be a reliable
method for mapping movement patterns in the Lumbar spine. (From Barrett et al, Man
Ther 1999; 4(2): 94-9).
11.8.3.2 Scoliosis
The study described in chapter 8 examined only the apical disc of the secondary lumbar
curve in subjects with idiopathic scoliosis. It would be of interest to extend this to
include all involved lumbar levels (Figure 11.2) and the primary thoracic curvature.
While this may pose imaging challenges with respect to MRI slice angles and the
difficulty in obtaining clear mid disc slices the results may be of value in predicting
curve progression and informing management choices.
Chapter 11: Conclusions and recommendations
Page XI-8
Figure 11.2: Proposed study examining involved levels beyond the apical segments of
the secondary lumbar curve in scoliosis by applying the same method with mid disc
transect (A), pixel samples across axial slice (B) for analysis of pixel intensity profiles
(C) and determination of NP deformation direction (D).
11.8.3.3 Herniated nucleus pulposus
Application of the described method to subjects with anular rupture and herniated NP
may provide data to inform clinical management of this condition with respect to the
effect of movement and positioning on extruded NP material (McKenzie & May, 2003).
Chapter 11: Conclusions and recommendations
Page XI-9
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Bogduk N, Lord S. A prospective study centralisation of lumbar and referred pain: a
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Donelson R, Aprill C, Medcalf R, Grant W. A prospective study of centralization of
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