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Morphology and pathoanatomy of the cervical spine facet joints in road traffic crash fatalities with
emphasis on whiplash – a pathoanatomical and diagnostic imaging study
PhD thesis
Lars Uhrenholt
Faculty of Health Sciences University of Aarhus
Institute of Forensic Medicine, University of Aarhus
Nordic Institute of Chiropractic and Clinical Biomechanics, Part of Clinical Locomotion
Science, University of Southern Denmark, Odense
Department of Neuroradiology, Aarhus University Hospital, Aarhus Sygehus (NBG)
Institute of Pathology, Aarhus University Hospital, Aarhus Sygehus (THG)
Morphology and pathoanatomy of the cervical spine facet joints in road traffic crash fatalities with emphasis on whiplash – a pathoanatomical and diagnostic imaging study Cover illustration Parasaggital histological section of a lower cervical spine facet joint illustrating a synovial fold. The thesis has been submitted to Faculty of Health Sciences, University of Aarhus, Aarhus, Denmark, in partial fulfilment of the requirements for the PhD degree. ©2007 Lars Uhrenholt Faculty of Health Sciences University of Aarhus Denmark Printed by SUN-TRYK, Aarhus 2007
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Preface
The present PhD thesis is based on the original work carried out in the period November 2002 to august
2007 at the Institute of Forensic Medicine, University of Aarhus in collaboration with the Nordic Institute
of Chiropractic and Clinical Biomechanics, Part of Clinical Locomotion Science, University of Southern
Denmark, Odense, the Department of Neuroradiology, Aarhus University Hospital, Aarhus Sygehus
(NBG) and the Institute of Pathology, Aarhus University Hospital, Aarhus Sygehus (THG).
The thesis has been submitted to the Faculty of Health Sciences at the University of Aarhus in order to
fulfil the requirements for attaining the PhD degree. The study was approved by the Scientific Ethics
Committee, Central Denmark Region, and The Danish Data Protection Agency.
All the material included in the work has been obtained at the Institute of Forensic Medicine, University of
Aarhus. Neuroradiological diagnostic imaging procedures have been conducted at the Department of
Neuroradiology, Aarhus University Hospital, Aarhus Sygehus (NBG). Macroscopical processing has
been performed at the Institute of Forensic Medicine, University of Aarhus whereas microtomal
sectioning has been performed at the Research Unit of Rheumatology and Bone Biology located at the
Department of Connective Tissue, Institute of Anatomy, University of Aarhus (formerly at the Institute of
Pathology, Aarhus University Hospital, Aarhus Sygehus (THG)).
The author sincerely appreciates the affiliations with the Nordic Institute of Chiropractic and Clinical
Biomechanics (NIKKB), Odense and the current part-time research position at the Institute of Forensic
Medicine, University of Aarhus. Financial support to the study has been generously granted from the
Foundation for the Advancement of Chiropractic Research, Denmark, the European Chiropractors Union
Research Fund (Grant # A.03-5), Switzerland, the Aarhus University Research Foundation, Denmark,
the Faculty of Health Sciences, University of Aarhus, Denmark, the A.P. Møller Foundation for the
Advancement of Medical Sciences, Denmark, the “Helga og Peter Kornings Fond”, Denmark and a
scholarship from the Spinal Research Institute of San Diego, USA.
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Acknowledgements
This thesis is the result of several years of fruitful collaboration between several institutes at the
University of Aarhus, Aarhus University Hospital and the Nordic Institute of Chiropractic and Clinical
Biomechanics (NIKKB), Odense and without the involvement of many people throughout its course the
completion of the thesis would not have been possible.
I would like to express my sincere gratitude to my chief-supervisor Markil Gregersen for giving me the
unique opportunity to explore a branch of forensic medicine, his genuine interest in the project and the
contributions, advices and support throughout the course of the project. Special thanks to my
supervisors, Annie Vesterby Charles, Edith Nielsen and Ellen Hauge who have all contributed immensely
in large periods of the project. I am grateful for your undeniable enthusiasm and positive approach to
solving many of the difficulties this project has encountered along the way. I would like to express my
deepest respects to my supervisor professor Flemming Melsen, DMSc. who sadly passed away
unexpectedly in the winter of 2004. Flemming Melsen contributed significantly to the original design and
concept of the project with his extensive experience in biology and pathology of cartilage and bone, and
his fantastic personality remains greatly missed.
The staff at the department of Neuroradiology, Aarhus University Hospital, Aarhus Sygehus (NBG) are
thanked for their enthusiastic commitment in the project. Without the logistic control of Niels Movim and
his administrative staff booking for diagnostic imaging would have been impossible as I always requested
timeslots within a few hours notice. This was furthermore supported by the staff on the ward that assisted
in a smooth and effective completion of each imaging session, including the nurses, porters,
radiographers and radiologists. A special thank goes to Vibeke Fink-Jensen who contributed with
unbiased second opinion evaluation of the diagnostic images.
My colleagues at the Institute of Forensic Medicine deserve a special acknowledgement. I appreciate the
skilful and professional cooperation of the forensic technicians who were engaged in the practical part of
this project – Karsten Mildahl Nielsen, Arne Nissen Ernst, Allan Laursen, Iuri Podgorbuschih and Jan
Schou. From the other side of the “barbed wire” the secretaries supported my endeavours emphatically
during the ever so necessary coffee break which coincidentally was also the most likely location to
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receive the invaluable computer support from Ole Lundskov. Particularly, Tove Hansen must be thanked
for the many hours she spent entering data into Epidata©. Furthermore, my small office enjoyed the
companionship of many different doctors during the last few years, with some of whom moments of
despair as well as exhilaration have been shared. Also the medical staff, who were so fortunate not to
share my office, deserve my compliments as they reinforced an excellent environment for scientific
research. A tremendous effort has been put into this project by Rita Ullerup at the Research Unit of
Rheumatology and Bone Biology. Her unique insight and experience in the fields of processing hard
tissue samples has been vital for the results and I appreciate the many occasions where we have shared
thoughts and sought for answers. Similarly, the discussions with Eva Olesen and Jytte Jakobsen
concerning histological problems and last minute decisions have always been of great use. Also thanks
to the Orthopaedic Research Laboratory, Aarhus University Hospital, for their assistance with laboratory
procedures when the time schedule was pressed to the limits.
The Research Unit of Rheumatology and Bone Biology, Aarhus University Hospital, has been a
formidable setting for discussion and presentation of preliminary findings which I have enjoyed. The
thoughtful and educative statistical counselling from Niels Trolle and Morten Frydenberg is greatly
appreciated as this allowed detailed evaluation of the large datasets. The support from NIKKB has been
important with Ulla Dinesen being the window of opportunity as she strictly managed the funding
obtained and finally the staff at Kiropraktisk Klinik Nortvig & Uhrenholt deserves my compliments for their
ever positive attitude despite my continuing changes in schedules.
To those who mean the most to me; my loving wife Hedvig and our dearest children Sofie and Sebastian.
To the fond memory of my mother.
Lars Uhrenholt
August 2007
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List of appended papers
The PhD thesis is based on the following papers:
I. Imaging occult lesions in the cervical spine facet joints
Lars Uhrenholt, Edith Nielsen, Annie Vesterby Charles, Ellen Hauge and Markil Gregersen
(Accepted for publication in American Journal of Forensic Medicine and Pathology)
II. Pathoanatomy of the lower cervical spine facet joints in motor vehicle crash fatalities
Lars Uhrenholt, Annie Vesterby Charles, Ellen Hauge and Markil Gregersen
Submitted
III. Histomorphology of the lower cervical spine facet joints
Lars Uhrenholt, Ellen Hauge, Annie Vesterby Charles and Markil Gregersen
(Submitted to Scandinavian Journal of Rheumatology, under revision)
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Abstract
A major issue in neck pain syndromes following road traffic crashes, including whiplash trauma, is the lack of
objectifiable organic injury in the majority of cases. Hence, detailed description of potential somatic injuries in the
cervical spine is necessary in order to improve differential diagnostics and therapeutic management strategies. The
present PhD study examined the lower cervical spine facet joints from 19 persons killed in road traffic crashes and
21 persons dead due to non-traumatic causes. Conventional X-rays, computed tomography, magnetic resonance
imaging, stereomicroscopy, and light microscopy were used. The aim was to examine whether discrete osseous and
soft tissue injuries could be detected in the lower cervical spine facet joints of road traffic crash fatalities, in
comparison to people who had died due to non-traumatic causes, using these techniques. The study showed that
discrete osseous lesions in the lower cervical spine facet joints could be detected by means of advanced diagnostic
imaging procedures, in particular using computed tomography, although approximately half of the unique discrete
facet fractures could not be detected. Soft tissue injuries including bleeding in the cervical facet joints and synovial
folds could not be determined reliably on any diagnostic imaging modality, including MRI, despite histological
evidence hereof. Furthermore, discrete non-fatal injuries were commonly identified in the road traffic crash fatalities,
including facet fractures, haemarthrosis, disruption and bleeding in the synovial folds. Pathology was best
appreciated on light microscopy in comparison to stereomicroscopic evaluation, and conventional autopsy
procedures did not reveal any of the injuries. Histomorphological examination showed that structural changes occur
early in life in both cartilage and subchondral bone. The most common findings were superficial flaking, horizontal
split and vertical fissures of the cartilage. The number of facets with flaking, horizontal split and osteophytes, and the
subchondral bone thickness increased with age. Males were generally more severely and frequently affected by
these changes than females. The presence of two synovial folds in each facet joint was documented irrespective of
age and gender. The calcified cartilage was found to be constantly equal to about 10 % of the total articular cartilage
thickness in all ages. Similarly, the articular facets were almost completely covered by hyaline cartilage with non-
covered bony edges being a rare finding.
In conclusion, this study has provided a detailed description of the histomorphology of the lower cervical spine facet
joints of a young population with regard to the soft tissues, cartilage and subchondral bone. It confirmed that there is
an under-representation of soft tissue injuries and discrete fractures in the cervical spine facet joints in people killed
in road traffic crashes examined by standardised autopsy and diagnostic imaging. It is possible that such injuries
may be present in casualties after non-fatal road traffic crashes, however the potential clinical implications of the
lesions identified in this study are not known.
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Dansk resumé
Et væsentligt problem med nakkesmerter efter trafikulykker, herunder whiplash traumer, er manglen på
objektiviserbare vævsskader i størstedelen af tilfældene. Af denne grund er en detaljeret beskrivelse af potentielle
vævsskader i halshvirvelsøjlen nødvendig for at forbedre diagnostik og behandlingsmæssige tiltag. Det nærværende
ph.d.-projekt undersøgte de nedre facetled i halshvirvelsøjlen fra 19 trafikdræbte og 21 personer døde af non-
traumatiske årsager. Der benyttedes konventionel røntgen, computer tomografi skanning, magnetisk resonans
skanning, stereomikroskopi og lysmikroskopi. Formålet var at undersøge om diskrete osseøse skader og
bløddelsskader kunne identificeres i halshvirvelsøjlens nedre facetled hos trafikdræbte til sammenligning med døde
af ikke-traumatiske årsager ved brug af disse teknikker. Studiet viste at diskrete osseøse skader i facetleddene
kunne identificeres ved hjælp af avancerede billeddiagnostiske teknikker, især computer tomografi, til trods for at
omkring halvdelen af alle unikke facetfrakturer ikke blevet opdaget. Bløddelsskader, inklusive blødning i ledspalten
og leddets folder kunne ikke sikkert bestemmes på nogen af de billeddiagnostiske teknikker, herunder magnetisk
resonans skanning, til trods for histologisk evidens for tilstedeværelse. Desuden fandtes diskrete ikke-dødelige
skader hyppigt hos de trafikdræbte, herunder frakturer af leddets facet, blødning i ledspalten, ødelæggelse af og
blødning i leddets folder. Skaderne kunne bedst identificeres ved lysmikroskopi til sammenligning med
stereomikroskopi, og konventionel autopsi kunne ikke identificere nogen af skaderne. Histomorfologisk undersøgelse
viste at strukturelle forandringer sker tidligt i livet i ledbrusken såvel som i den subkondrale knogle. De hyppigste
fund var overfladisk fibrillation, horisontale og vertikale revner/fissurer i ledbrusken. Antallet af facetter med
overfladisk fibrillation, horisontale revner og osteofytter, og den subkondrale knogletykkelse steg med alderen.
Mænd var påvirket hyppigere heraf og i sværere grad end kvinder. To synoviale folder blev identificeret i hvert
facetled uafhængigt af køn og alder. Den forkalkede ledbrusk var konsekvent omkring 10 % af den totale tykkelse af
ledbrusken i alle aldre. Ligeledes var ledfacetterne næsten fuldstændigt dækkede med hyalin ledbrusk og udækkede
knogleender var sjældne.
Sammenfattende har dette studium bidraget med en detaljeret beskrivelse af halshvirvelsøjlens nederste facetleds
histomorfologi i en ung population, med hensyn til bløddelene, brusken og den subkondrale knogle. Det blev
bekræftet, at der er en under-rapportering af bløddelsskader og små frakturer i halshvirvelsøjlens facetled hos
trafikdræbte undersøgte ved konventionel autopsi og billeddiagnostisk undersøgelse. Det er muligt at sådanne
skader også kan være til stede hos tilskadekomne efter ikke-dødelige trafikulykker, men de mulige kliniske
betydninger af læsionerne identificeret i dette arbejde er ikke kendte.
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Content
1. Introduction 15
1.1. Aim 17
2. Types of cervical spine trauma during road traffic crashes 18
2.1. High energy crashes 18
2.2. Low energy crashes – whiplash trauma 18
2.2.1. Pathomechanics of the cervical spine during whiplash trauma 19
2.2.2. Incidence rates of acute whiplash injury 19
2.2.3. Risk of acute whiplash injury 21
2.2.4. Risk of chronic whiplash symptoms 21
3. Anatomy and degenerative changes of the cervical spine 22
3.1. The cervical spine 22
3.2. Anatomy of the lower cervical spine facet joints 24
3.2.1. Histology and histomorphometry of the cervical spine facet joints 26
3.2.2. Degenerative and age-related changes of the cervical spine facet joints 28
3.2.3. Grading and staging of osteoarthritis of the cervical spine facet joints 28
4. Pathology of the cervical spine after road traffic crashes 30
4.1. Fatal injuries in fatal road traffic crashes 30
4.2. Non-fatal injuries in fatal road traffic crashes 32
4.3. Injuries following survivable road traffic crashes 32
4.3.1. Whiplash injury 32
5. Diagnostic imaging of the cervical spine after road traffic crashes 36
5.1. Imaging modalities 36
5.2. Fatal road traffic crashes 37
5.3. Survivable road traffic crashes 38
6. Materials and methods 39
6.1. Materials 39
6.2. Retrieval of specimens 39
6.3. Diagnostic imaging procedures 40
6.3.1. The first examination of the radiological images 40
6.3.2. The second examination of the radiological images 41
6.3.3. The third examination of the radiological images 41
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6.4. Histolaboratory procedures 41
6.4.1. Production of the 3-mm thick anatomical slices 43
6.4.2. Examination of the 3-mm thick anatomical slices 43
6.4.3. Production of the 10 μm thick histological sections 45
6.4.4. Examination of the 10 μm thick histological sections 45
6.4.5. Handling of data from the 10 μm thick histological sections 47
6.4.6. Evaluation of the inter- and intraobserver agreement of the morphological findings 51
6.5. Police records and information from the medico-legal autopsy 51
6.6. Statistical analysis 51
7. Summary of results 53
7.1. Diagnostic imaging findings (Paper I) 53
7.2. Pathological findings (Paper II) 58
7.3. Anatomical and age-related findings (Paper III) 62
7.4. Other findings 68
7.4.1. Inter- and intraobserver agreement 68
7.4.2. Police records 68
8. Discussion 70
8.1. Diagnostic imaging of the cervical spine facet joints after trauma 70
8.2. Pathology of the cervical spine facet joints after trauma 72
8.3. Anatomy of the lower cervical spine facet joints 74
8.4. Methodological considerations 76
8.5. External validity and clinical implications 80
9. Conclusions and perspectives 83
10. References 85
Appendices 105
Papers
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List of abbreviations
BAC Blood alcohol concentration
CT Computed tomography
IAP Inferior articular process
LOSRIC Low speed rear-impact collision
MMA Methylmethacrylate
MRI Magnetic resonance imaging
OA Osteoarthritis
RTC Road traffic crash
SAP Superior articular process
WAD Whiplash-Associated Disorders
V Velocity change (Delta-V)
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List of figures
Figure 2.1 Segmental pathokinematics with segmental hyperextension “S-shape”
Figure 3.1 The cervical spine
Figure 3.2 Overview of the lower cervical spine facet joint structures
Figure 3.3 The arcadial and zonal organisation of articular cartilage of a cervical spine facet
Figure 4.1 Lesions reported in humans subjected to cervical acceleration-deceleration trauma
Figure 6.1 Illustration of a cervical spine specimen
Figure 6.2 Illustration of the sawing of 3-mm thick slices from a cervical spine specimen
Figure 6.3 Setup for histomorphometric measurements
Figure 6.4 Histomorphometric quantitative measurements
Figure 6.5 Random location of histomorphometric measurements
Figure 7.1 Discrete injuries to the cervical spine facet joint soft tissue structures
Figure 7.2 Cervical spine facet fracture in a motor vehicle crash fatality
Figure 7.3 Injuries to the cervical spine facet joint in a motor vehicle crash fatality
Figure 7.4 Haemarthrosis in a cervical spine facet joint in a fatal motor vehicle crash victim
Figure 7.5 The morphological variables
Figure 7.6 Complete covering of the articular surface by the synovial folds
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List of tables
Table 4.1 The Quebec Task Force grading system of Whiplash-Associated Disorders (WAD)
Table 6.1 Description of the morphological and histomorphometric variables
Table 7.1 Subjects with unique facet fractures on either histology or CT consensus
Table 7.2 Histopathological findings in the road traffic crash fatalities
Table 7.3 Morphological findings of the lower cervical spine articular facet
Table 7.4 Histomorphometric findings of the lower cervical spine articular facet
Table 7.5 Inter- and intraobserver agreement regarding microscopy of morphological variables
xiv
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1. Introduction
Each year several millions of people are injured in road traffic crashes (RTC) world-wide with an
estimated 1.7 million injuries and more than 40.000 fatalities in Europe alone, although the figures are
declining 1-3. In Denmark, the official total number of injured people recorded by the police was 6.588 with
331 people killed in 2005. In comparison to the “White Paper” published in 2001 by the European
Communities on road traffic safety 2, the Danish figures are approximately equivalent to a reduction of 34
% and 28 % in fatalities and casualties respectively over the first five-year period (2000 – 2005) and thus
fulfils the part-requirements of the White Paper 4.
Despite the overall positive development, the number of relatively slight or minor injuries following RTC’s
have been reported to be increasing, particularly involving whiplash injury which is the most common
“minor” injury following RTC’s 5-10. In Denmark, a conservatively estimated 6.000 new cases of whiplash
injuries occur each year 11. Whiplash injuries, and in particular related symptoms in and from the neck,
are responsible for substantial morbidity with adverse effects on the quality of life for the affected
individuals as well as large health care expenditures 1;2;11-17. The exact costs related to whiplash injuries
are unknown, however the annual costs in the United States has been estimated to be in the range of
billions of US dollars annually 18;19. In Western Europe the annual costs have been estimated to be 8
billion Euros each year 20, and in Sweden the expected future costs related to one years casualties has
been estimated to four billion Swedish Kroner 12.
The most common symptom after whiplash injury is neck pain and the cervical spine facet joints have
been found to be closely related to persistent symptoms based on several clinical studies of patients
suffering from chronic symptoms after whiplash injury 21-25. Post-mortem studies have identified
pathoanatomical lesions in the cervical spine in both people suffering from chronic neck pain after
survivable road traffic crashes 26-29, and fatal road traffic crashes with high incidence rates of lower
cervical spine facet joint injuries 30-32.
In many cases the exact cause of the patient’s symptoms after whiplash injury cannot be established and
currently no pathognomonic whiplash injury has been identified. Despite the fact that a possible
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explanation of the most common acute symptoms after whiplash injury can be found in organic pathology
of lower cervical spine facet joints in whiplash patients, the knowledge of tissue injuries following
whiplash trauma is limited and remains inconclusive for the majority of whiplash related conditions 14;24;33-
35. Similarly, only few controlled post-mortem studies have examined the incidence rates of specific
lesion types in these joints 31;32;36. If injuries are identified in these joints in people killed in road traffic
crashes this may support the theories of an underlying organic cause of symptomatology in subgroups of
whiplash patients 30;33;34;37;38.
Conventional X-ray studies of the lower cervical spine facet joints of whiplash patients rarely report
pathological findings, and fractures of the articular columns have usually been identified in severely
injured patients 39-41. In a number of imaging studies of acutely injured whiplash patients using magnetic
resonance imaging (MRI) injuries have been identified primarily in the intervertebral discs and correlating
the findings with the symptoms and the preceding trauma have been found difficult in many cases 42-45.
However, none of these studies have evaluated the cervical spine facet joints in any great detail. In
several studies of people killed in road traffic crashes, examined with conventional X-rays, computed
tomography (CT) and MRI, the diagnostic imaging procedures have only identified a small part of
pathological lesions that were observed microscopically in the lower cervical spine facet joints 30-32;36;46.
Despite these inconclusive results no studies have evaluated the cervical spine facet joints in detail,
including correlating findings from microscopy with diagnostic imaging. Furthermore, the interobserver
agreement of the diagnostic imaging examinations of cervical spine facet has not been tested in a
blinded and controlled fashion. Hence, the incidence rates of injuries to the cervical spine facets detected
on diagnostic imaging, the correlation of these findings to microscopy and the reliability of the radiological
evaluations have not been vigorously tested.
Numerous studies have investigated the cervical spine morphology and histomorphometry including the
properties of the articular facets and their soft tissues 47;48;48-56. However, quantitative data regarding the
properties of the hyaline cartilage, calcified cartilage and subchondral bone of the cervical spine facets is
very limited 48.
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1.1. Aim
It was hypothesised that there is an under-representation of pathoanatomical lesions in the cervical spine
facet joints in people killed in RTC’s examined by standardised autopsy and conventional radiological
evaluation.
The primary aim of the present PhD thesis was to investigate whether discrete lesions in the lower
cervical spine facet joints could be detected in people killed in a passenger car crash by advanced
diagnostic imaging procedures, including conventional X-rays, CT and MRI, and specialised
microscopical evaluation as compared to non-traumatized decedents. The morphology of the lower
cervical spine facet joints in a group of young individuals (age 20-49 years) should be evaluated
qualitatively and by histomorphometry. Furthermore, attempts were made to compare the pathological
findings in the people killed in the passenger car crashes with data from the police records with regard to
mechanism of trauma.
The ultimate goal was to improve our knowledge of discrete spinal injuries in road traffic crash victims
which may help improving diagnostic and therapeutic possibilities in survivors of RTC’s sustaining non-
fatal injuries to the cervical spine facet joints.
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2. Types of cervical spine trauma during road traffic crashes
There are an infinite number of possible types of RTC’s. With the purpose of broad classification these
are often described according to the direction of first impact (which relates to the primary direction of
force) and severity as it relates to the relative energy transfer (high energy versus low energy crashes),
which is often referred to as high speed and low speed crashes respectively.
2.1. High energy crashes
Far the majority of fatal car crashes involve high energy transfer to the decedent as a consequence of a
high speed crash involving a single vehicle in a rollover or a frontal collision between two vehicles 57-59.
However, other vectors are also implicated in fatal crashes, for example the American National Highway
Traffic Safety Administration found that 6.5 % of people killed in passenger car crashes in the United
States were killed in a rear-impact collision in 2005 58. The mechanics of injury in high energy crashes
are often complex with multiple different types of injurious loading of the occupants 60;61. The exposure of
high energy load over a short time-span carries a high risk of serious bodily injury which is characteristic
of high speed crashes, with the risk of serious injury and death being closely related to the velocity
change ( V) as a function of time, i.e. acceleration, of the involved vehicles and occupants 57;59.
2.2. Low energy crashes - whiplash trauma
In contrast to high speed RTC’s, low speed crashes (low energy crashes) are far more common. The
majority of all injurious crashes take place with velocity changes below 30 km/hour 14;59;62-65. The classical
whiplash trauma is a low speed rear-impact collision (LOSRIC), where the collision between two vehicles
exposes the driver and/or passengers of the “target” vehicle to a biphasic acceleration-deceleration force
loading with principal inertial loading of the occupants, i.e. without head strike 14;59. However, other types
of trauma, e.g. motor vehicle collisions involving head strike, skiing accidents and assaults, are regularly
classified as whiplash trauma due to similar symptomatology which makes the group of whiplash patients
heterogeneous affecting the efficiency of clinical classification systems, e.g. the WAD-grading system 66.
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2.2.1. Pathomechanics of the cervical spine during whiplash trauma
The early whiplash models hypothesised that the most injurious mechanism involved hyperflexion and in
particular hyperextension of the cervical spine during rear-impact 67. Later more complex kinematics
were identified and the observations were described as a “serpentine configuration” of the cervical spine
during a rear-impact collision 68. However, it was not until the mid-1990’es that experiments using human
volunteers and post-mortem human subjects identified segmental biphasic pathomechanics during
experimental indirect rear-impact acceleration loading 69;70. Biomechanically these rear-impact collisions
usually take place within a timeframe of approximately 150 milliseconds, during which the occupants are
exposed to well-described patterns of kinematics. This involves forward acceleration of the torso with
ramping causing compression of the cervico-thoracic spine and potentially pathophysiological segmental
movements of the cervical spine due to changes in the instantaneous axis of rotation. Consequently,
shear, compression and distraction loading of particularly the facet joints takes place with the
simultaneous “s-shape” configuration of the cervical spine (Figure 2.1) 69-74.
The abnormal kinematics are potentially injurious to the regional anatomical structures as the normal
anatomical boundaries of mobility are exceeded within the first 75-100 milliseconds of the collision
14;19;37;70;75;76. This has recently been supported in biomechanical experiments where the facet joint
capsular ligaments and adjacent soft tissues are at risk of injury at acceleration forces typical for low
speed rear-impact collisions 73;77-81. Since the kinematic changes take place very early on during
physiological loading there is no or only limited protective reflex contraction of the neck muscles 37;82;83,
and as the pathophysiological movements take place within the normal range of motion there is often no
global hyperextension or hyperflexion of the cervical spine 14.
2.2.2. Incidence rates of acute whiplash injury
Despite the recent decrease in the number of people killed and severely injured in RTC’s in most
European countries there appears to have been an increase in the number of people sustaining non-fatal
injuries 7;10. The incidence rates of whiplash injuries have not been confidently established, probably due
to differences in sampling systems and geographical and cultural differences. However, incidence rates
have been estimated in several countries ranging from 10 per 100.000 of the general population of New
Zeeland 84, 70 per 100.000 inhabitants annually in the province of Quebec (Canada) 66, 417 per 100.000
inh
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Figure 2.1 Segmental pathokinematics with segmental hyperextension ”S-shape”
The normal correlation in the cervical spine facet joint (A). During typical rear-impact loading (i.e. loading from the
posterior) the cervical spine undergoes a segmental pathophysiological hyperextension “S-shape” associated with
shear forces, compression forces posteriorly and distraction forces anteriorly acting on the joint structures (B).
21
inhabitants in the United Kingdom 7 to as high as 1.172 per 100.000 inhabitants annually in USA 14. In
Denmark, an estimated 120 per 100.000 inhabitants sustain a whiplash injury each year 11;85. However,
since most of the official figures are based primarily on police records and hospital admission records
they must be regarded with caution. Under-reporting of injuries sustained in crashes with limited or no
property damage is likely as these crashes are rarely attended by the police. Furthermore, hospital
admission records do not include injured people contacting the general practitioner or other
physicians/therapist’s directly, as well those people not contacting any medical personnel 86;87.
2.2.3. Risk of acute whiplash injury
Although the most common form of whiplash injury carry a remote life-threatening potential, a substantial
risk of acute injury (here defined as relevant symptoms after the trauma) is present and relates to multiple
crash- and personal related factors 14;59. The immediate risk of sustaining an acute whiplash injury after a
whiplash trauma is approximately 30-60 % 14;18;88-90, with a wide range of severity of symptoms,
developing most often within the first 48 hours of the crash, although delayed onset of symptoms has
been reported 14;91-94. As a combination of crash severity parameters and individual susceptibility to injury,
which if affected by biological variability, uniquely relates to the outcome of any given crash, no
generalised injury threshold has been established for low speed crashes 88;95-97.
2.2.4. Risk of chronic whiplash symptoms
Approximately 33-43 % of the originally injured subjects in a whiplash trauma develop longstanding
symptoms of varying severity 18;91. Notwithstanding these figures, official figures from several countries,
including the National Board of Health in Denmark, estimate that the risk of developing chronic symptoms
in Denmark is below 5 % 11, and Swedish risk figures range between 5-10 % 98. The inconsistencies
between international publications and the official national figures are furthermore troublesome taking into
consideration recent results from prospective studies of Danish whiplash injuries in which persistent
symptomatology at one year after injury were reported in approximately 50 % of the patients 13;99. The risk
of sustaining chronic disabling symptoms that affects the working ability has recently been found to be as
high as 12 % 17;99 and 25 % 13 in two independent prospective studies. Although the term disability is not
uniquely defined in all studies, similar reports of lower percentages of long-term disability have previously
been described 100-105.
22
3. Anatomy and degenerative changes of the cervical spine
The cervical spine consists of seven vertebrae, with the two upper vertebrae; atlas (C1) and axis (C2)
being atypical vertebrae and the remaining five vertebrae (C3-C7) being classified as typical vertebrae.
The vertebral bodies of atlas and axis have unique anatomical appearances and consequently unique
biomechanical properties. In the lower cervical spine (C3-C7) osseous elements extends posteriorly from
the vertebral bodies, consisting of pedicles, articular columns, transverse processes, laminae and
spinous processes (Figure 3.1). The primary functions of the cervical spine are to supply support and
mobility to the head and provide protection to the spinal cord.
3.1. The cervical spine
With the exception of occiput-C1 and C1-C2, each cervical vertebral body is connected to each other by
an intervertebral disc which is bordered postero-laterally by the uncinate processes forming the
uncovertebral joints of Luschka 49;106;107. Posteriorly the facet joints of the articular columns supplements
to the mobility and stability of the cervical spine and guide weight bearing. The cervical spine mobility is
highly specialised depending on the anatomical location 108-110. In the upper cervical spine the primary
movement between occiput-C1 is flexion/extension and between C1-C2 it is rotation 108. In the lower
cervical spine all vertebral levels contribute to flexion, extension, rotation and lateral flexion although
some segments are more active than others 108;109. Ligaments are widely dispersed in the cervical spine
and their appearance reflects their supportive function. In the upper cervical spine the principal ligaments
are the transverse ligament, the apical ligament, the alar ligament, the capsular ligaments and the
anterior and posterior atlanto-occipital membrane. These ligaments check movement and are
responsible for limiting motion thereby adding stability. In the lower cervical spine the primary ligament
are the anterior and posterior longitudinal ligaments, the ligamentum flavum, the interspinous ligaments
and the capsular ligaments. Surrounding the skeletal cervical spine, uniquely specialised musculatures
add function to the highly mobile region. In the upper cervical spine the suboccipital muscles control
mobility in combination with the sternocleidomastoideus, trapezius and some of the deeper neck
23
Figure 3.1 The cervical spine
The cervical spine is illustrated in overview from the side with a typical vertebra shown from superior and the
lateral aspect.
24
muscles. In the lower cervical spine muscles controlling mobility include primarily the scaleneus group,
the levator scapulae, the trapezius and the anterior flexor muscles. There is an intricate nerve supply to
the cervical spine. Nerves from the cervical and brachial plexus divide in branches supplying the cervical
spine bones, ligaments, intervertebral discs, muscles and other soft tissues in a segmental organisation.
Autonomic fibers, relaying in the cervical sympathetic ganglion and coursing with the vasculature as well
as arising from the spinal nerves, also supply some of the cervical spine structures. The blood supply to
the cervical spine arises primarily from the brachio-cephalic trunk, the common carotid arteries and the
vertebral arteries. Spinal and muscular branches supply the vertebral bodies, the posterior elements and
the adjacent musculature of the posterior part of the cervical spine.
3.2. Anatomy of the lower cervical spine facet joints
The lower cervical spine (C3-C7) facet joints are arranged in pairs bilaterally and each joint consist of
opposing articular facets, i.e. the inferior articular process (IAP) of the vertebra above and the superior
articular process (SAP) of the vertebra below (Figure 3.1). The facets are oriented slightly oblique to the
saggital plane, with the superior articular facets facing laterally and upwards approximately 45o to the
horizontal plane, with gradual changes in orientation in the cervico-thoracic transitional zone. The
articular facets are covered completely or in part by hyaline cartilage as the presence of cartilage free
areas, i.e. “cartilage gaps”, have recently been identified (Figure 3.2) 48. The facet joint capsules are
loose and thin with the strongest part in the antero-lateral aspect. Medially the capsular fibers are
contiguous to those of the ligamentum flavum and the weakest fibers are in the dorsal region 107;111. The
posterior joint capsule is supported by the attachment of the multifidus muscles at all levels 107. The
presence of synovial folds (fat pads, meniscoids or inclusions) of the anterior and posterior margins of
the lower cervical spine facet joints have been described inconsistently in several anatomical studies
(Figure 3.2) 49;111-115. A recent review noted that these structures are present as small vascular synovial-
lined fat pads, although no mentioning to the exact prevalence was noted 107, however one study have
identified meniscoids in all facet joints of 20 spines from decedents aged 20 to 80 years 116, and another
study identified anterior and posterior meniscoids in all six facet joints from one subject examined with
microscopy and high-field magnetic resonance imaging 117. The exact function and importance of the
synovial folds is not clearly understood. Immediately anterior to each facet joint the cervical spine nerve
root exits the spinal canal through the intervertebral foramen formed by the pedicles, vertebral bodies,
25
Figure 3.2 Overview of the lower cervical spine facet joint structures
Three facet joints from the lower cervical spine illustrated with two different staining techniques (Masson-Goldner
trichrome and Safranin-O fast green) showing hyaline cartilage (a), an anterior synovial fold (b), a posterior joint
capsule (c), and a nerveroot (d) on selected joints, original magnification x1.
26
intervertebral disc and the articular column 106;107;118. At each spinal segment the recurrent (spinal)
meningeal nerve of Luschka re-enters the spinal canal via the foramen in order to supply the outer part of
the intervertebral disc with sensory and sympathetic autonomic fibers. The medial branches and
accessory nerves of the primary dorsal rami supply the articular structures, including the bone,
musculature, capsule and synovial folds, but not the articular cartilage, with nociceptive fibers and
mechanoreceptive nerve endings at a segmental organisation 119;120. Each medial branch curves the
ipsilateral articular column and sends ascending and descending branches to the joints above and below
121. The spinal and accessory branches of the vertebral arteries anastomise longitudinally and course the
intervertebral foramen where they continue as anterior and posterior radicular arteries with vascular
supply to the facet joints, spinal cord and posterior elements of the spinal column and are surrounded by
the accessory vertebral vein 106.
3.2.1. Histology and histomorphometry of the cervical spine facet joints
The general histological appearance of human synovial joints, including the cervical spine facet joints,
has been described in detail 47-50;122;123. The hyaline cartilage covering of the cervical spine facets exhibit
the typical arcadial appearance (Bennington’s arcades) of cartilaginous matrix with zonal distribution
(Figure 3.3), although this is not always readily identified, e.g. at the periphery of the joint. The function of
the cartilage is to increase the area of load distribution and provide a smooth surface for mobility 122;124.
Articular cartilage is composed of more than 70% water and only 5% of the total volume is accounted for
by the chondrocytes 122-124. The major constituents of the extracellular matrix are the collagen type II and
proteoglycan aggrecan 122-124. Histomorphometrical evaluations of the cervical spine facets have been
performed and data are available concerning the anatomical properties of the posterior articular columns
and the orientation of the cervical facets 51-53;56. In macroscopical studies the facet joint width, as
measured in the coronal plane, has been measured to be about 11-12 mm 48;55 and the depth in the
saggital plane to be about 10 mm 55. The mean area of the inferior articular surfaces have been found to
increase from approximately 1.25 cm2 at C3 to 1.6 cm2 at C7 125. The mean overall thickness of the
cervical spine facet cartilage has been shown to be somewhat smaller in females (0.4 mm) compared to
males (0.5 mm) based on a cryomicrotomal study 48. In joints, other than the cervical spine facet joints,
the thickness of the calcified cartilage has been found fairly constant occupying approximately 5 % (3-
8%) of the total cartilage thickness 126-129. Apparently, no detailed histomorphometric information exists of
27
Figure 3.3 The arcadial and zonal organisation of articular cartilage of a cervical spine facet
Overview of a facet, original magnification x4 (A). Zonal organisation of the cartilage with the hyaline cartilage
divided into a superficial, middle and deep zone, original magnification x10 (B). Stained with Masson Goldner-
Trichrome.
28
the quantitative properties of the cartilage and subchondral bone of the lower cervical spine facets.
3.2.2. Degenerative and age-related changes of the cervical spine facet joints
The facet joints and the articular cartilage are likely to degenerate as a consequence of overuse and
repeated injury as well as ageing 49;107;122;130;131. However, it is important to note that osteoarthritis of the
facet joints is not necessarily a consequence of ageing, and that these joints are frequently unaffected in
spondylosis 49;106.
Generally, degeneration of the cartilage takes place over time, where the initial changes consisting of
only discrete superficial flaking (fibrillation) of the cartilage are gradually replaced by more aggressive
changes in the shape of vertical fissures, erosions, denudation and deformation 49;107;122;123;131. As a
consequence of the degenerative process the changes are most vividly visualised in the unmineralised
hyaline cartilage, but changes also take place in the calcified cartilage as well as the subchondral bone
which undergoes remodelling 122;127;129;132. Vascular invasion through the basophilic tidemark (the border
between the unmineralised hyaline cartilage and calcified cartilage) with increasing duplications of the
tidemark, has been related to ageing 122;133. New bone formation in the shape of osteophytes may
develop at the borders of the joints and cysts may form in the subchondral region 49;106;122;127;133. Hence,
age-related changes in the facet joints are generalised affecting the osseous, cartilaginous and the soft
tissue structures.
3.2.3. Grading and staging of osteoarthritis of the cervical spine facet joints
General histological classification and grading systems are available for the description of human joints
49;130;131;134-136. However, these are primarily based upon the examination of large joints, such as the hip
and knee joints and have not been validated for the use in the lower cervical spine facet joints, with the
exception of recent classification systems, some of which have been developed for the lumbar spine
facet joints 130;134;135;137. Grading of osteoarthritis of the cervical spine facet joints is made difficult by the
lack of a validated system for histological grading of these joints, although several general classification
systems are available 49;123;130;131;134-137.
A grading system has been developed for the lumbar spine facet joints, and has recently been utilized in
the evaluation of the cervical spine 130;135;137. However, it is questionable whether this grading system
supplies a valid interpretation of the true extent of degenerative changes as differentiation between
29
grades of severity is difficult. Recently, an important paper assessed current knowledge based on large
joints and proposed a system that takes into consideration both the grade (extent of widespread
changes) and the stage (severity) of the OA changes 131. Although this system is based on the evaluation
of large joints, and it has not been tested on smaller synovial joints such as the cervical spine facet joints,
it seems suitable for the examination of facet joints.
30
4. Pathology of the cervical spineafter road traffic crashes
By the Quebec Task Force on Whiplash-Associated Disorders (WAD) classification, whiplash is
classified according to the clinical presentation and the clinical findings (Table 4.1) 66. In case of severe
injuries such as brain injuries, cervical spine fracture or spinal cord injury, the grading is not applicable.
Hence, studies evaluating the clinical consequences of whiplash injuries most often refer to subjects
graded as WAD II or III, and the implications of WAD IV has not been investigated in great detail.
Therefore, somatic injuries have rarely been reported in studies of people sustaining whiplash injury
probably due to that fact that evidence of tissue damage often excludes participation in these studies
whereby the included subjects most often are graded WAD II. Hence, in subgroups of whiplash injured
subjects (e.g. WAD III and WAD IV) the structural integrity of relevant anatomical structures has not been
evaluated in detail which may have implications, not only for the management of these patients, but also
influence management strategies and utilization of diagnostic procedures in apparently less severely
injured people (e.g. WAD II).
4.1. Fatal injuries in fatal road traffic crashes
Far the most common non-survivable types of injuries are those related to the head- and cervical spine
complex. Injuries to the cervical spinal cord, brainstem and brain are often not survivable, and in many
cases part of complex injury patterns. Other fatal injuries include for example cardiac tamponade,
disruption of the aorta and severe contusion injuries of the pulmonary tree 60;138. Generally, the
decedents have in common, that they suffer several types of injuries to different body parts, and that
often several competing causes of death are present. The primary role of the medico-legal autopsy is to
identify and describe all injuries sustained by the decedent and conclude upon the cause/causes of
death 60;138. Hence, registration of fatal and non-fatal injuries is an important role of the medico-legal
autopsy.
31
Grades of severity Clinical presentation
0 No neck complaints; no physical sign(s)
I Neck pain, stiffness, or tenderness only; no physical signs
II Neck complaints AND musculoskeletal sign(s)*
III Neck complaints AND neurological sign(s)**
IV Neck complaints AND fracture or dislocation
*: Musculoskeletal signs include decreased range of motion and point tenderness
**: Neurological signs include decreased or absent deep tendon reflexes, weakness, and sensory deficits
Table 4.1 The Quebec Task Force grading system of Whiplash-Associated Disorders (WAD)
32
4.2. Non-fatal injuries in fatal road traffic crashes
Minor injuries after fatal road traffic crashes are not always described in same detail as severe injuries,
and discrete injuries may not be readily visualised during standardised autopsy 30;32;139;140. In the cervical
spine this is particularly true for micro-fractures, haemarthrosis and injuries to the facet joints,
intervertebral discs, ligaments and muscles 27;28;30-32;36;46;139;141.
4.3. Injuries following survivable road traffic crashes
A wide range of lesions have been reported in humans subjected to survivable road traffic trauma,
including cervical acceleration-deceleration trauma, i.e. also whiplash trauma (Figure 4.1) 14.
Furthermore, post-mortem studies of people previously suffering from chronic neck pain after road traffic
crashes have identified pathoanatomical lesions in the cervical spine that may have been caused by the
preceding trauma and have had clinical relevance for the decedents prior to death 26-29. It has been
shown that these lesions by in large are identical to those lesions identified in several post-mortem
studies of people killed in fatal road traffic crashes 30, and that injuries to the facet joints are particularly
common in the lower cervical spine 31;32. Although interesting, it is not known what relevance these post-
mortem findings have in comparison to injuries sustained in survivable road traffic crashes, and uncritical
extrapolation of autopsy findings to clinical settings is not admissible 19;30;33. Nonetheless, it seems likely
that in some cases injuries are sustained in survivable road traffic crashes that are similar to those
identified at post-mortem 30;33;34;38, and it has previously been suggested that convergent validity is
constituted by the fact that neck pain is common, particularly following whiplash injury to the cervical
spine and that discrete injuries to the cervical spine is common in post-mortem subjects killed in road
traffic crashes 34.
4.3.1. Whiplash injury
The exact cause of the patient’s symptoms after whiplash injury has not been established and currently
no pathognomonic whiplash injury has been identified. Hence, the definition of whiplash injury does not
include the description of an organic lesion in the cervical spine. Rather, the term whiplash injury refers
to the mechanism of trauma. Hence, a prerequisite for a whiplash injury is the exposure to a preceding
whiplash trauma, which can be strictly defined as an acceleration-deceleration trauma during a motor
vehicle collision, although other mechanisms of trauma have been known to cause similar sympt
33
Figure 4.1 Lesions reported in humans subjected to cervical acceleration-deceleration trauma
(Illustration modified from Foreman et al. 14)
34
vehicle collision, although other mechanisms of trauma have been known to cause similar
symptomatology 14;59;66. More recently the alternative term; Whiplash-Associated Disorders (WAD), has
been proposed together with a whiplash injury grading system (Table 4.1) 66. However, although the
WAD grading system allows some considerations regarding the severity of injury, the grading is primarily
related to the cervical spine and does not consider other signs or symptoms, e.g. lumbar spine pain.
Similarly, casualties eligible for the WAD grading IV, e.g. cervical spine fractures with spinal cord
compromise, are rarely scored according to the WAD grading system as their injuries are often life
threatening with consequently different therapeutic considerations 142. Nonetheless, the WAD-system
has some justification as the most common symptom following a whiplash injury is neck pain 14;21;59;66;142-
145. Since different directions of crash impulses, e.g. frontal versus rear-impact, causes different
interactions throughout the human body, and thereby carries different tissue damage and injury potential,
these parameters should be integrated in the diagnostic possibilities 14, and the duration of symptoms
and stage of recovery should also be more specifically incorporated 66;146. This was actually proposed in
an earlier cervical acceleration-deceleration classification system, published prior to the WAD grading
system 146;147.
In theory, acute neck pain can be explained by somatic injury, such as sprain/strain of cervical spine soft
tissues, contusion of articular structures, disruption of the cervical discs, damage to nerve roots and
microfractures of osseous structures (Figure 4.1) 24;33-35, however, it remains unclear to what extent these
injuries may apply to whiplash patients. Similarly, the exact mechanism of sustained chronic pain in the
cervical spine after whiplash is unclear, although it has been shown that alterations in the central
processing of sensory stimuli (central hypersensitivity) may be present 148-150. Such conditions are
thought to affect, not only the brains interpretation of ascending nociceptive information, but also
influence the segmental circuits on a spinal cord level whereby the patients’ experience of pain is altered
148-151. Alternatively, other non-organic underlying causes have been proposed with the bio-psychosocial
model and post-traumatic stress disorder defining the symptoms’ origin and maintenance as primarily
psychogenic 152-155.
The most common symptoms following an acceleration-deceleration injury are neck pain and headache
14;21;59;66;142-145 and the cervical spine facet joints have been found to be closely related to chronic neck
pain based on several clinical studies of patients suffering from chronic symptoms after whiplash injury 21-
25. Furthermore, several studies have found that abolishing the nerve supply to these joints, by nerve
35
blocks, radiofrequency neurotomy or intra-articular prolotherapy, neck pain may be alleviated for periods
of months 156-160. Hence, the cervical spine facet joints have high priority in the diagnostic evaluation of
whiplash patients. However, despite extensive research into the mechanisms of trauma and clinical
parameters, the knowledge of tissue injuries in the cervical spine facet joints following whiplash trauma is
limited and remains inconclusive for the majority of whiplash related conditions.
36
5. Diagnostic imaging of the cervical spine after road traffic crashes
5.1. Imaging modalities
In the diagnostic evaluation of victims from road traffic crashes the most commonly utilised diagnostic
imaging modalities include conventional X-rays, CT and MRI. For the purpose of screening for skeletal
injury after trauma, the American College of Radiology have proposed in their appropriateness criteria 161
that conventional X-rays are recommended as the primary choice of screening 162;163. However, the
appropriateness of any specific radiological examination is made by the referring physician and
radiologist in light of the particular circumstances for any given case 161. Hence, in increasingly severe
injuries CT is more likely chosen as the primary tool of screening if there is clinical indication of cervical
spine fractures 161;164-169.
Conventional X-rays are the most commonly utilised diagnostic imaging procedures for the screening of
injuries following trauma worldwide 162;170. The advantage of conventional X-rays is that it is
geographically easy accessible around the world, it is cost-efficient and it does identify orthopaedic
damage, e.g. extremity fractures, tumors and foreign objects. However, soft tissue injuries and minor
fractures are often not detectable on conventional X-rays. Furthermore, radiation safety must be
considered every time a patient is exposed to an X-ray exam 171;172.
Computed tomography is particularly sensitive towards detection of skeletal injury because of its
unparalleled resolution and illustration of bony detail and is therefore used extensively in the diagnostic
evaluation of severely injured casualties 14;164;167. Furthermore, CT allows good appreciation of
abdominal, thoracic, and pelvic organs as well as the brain. The accessibility to CT-scanners is good in
developed countries, and as the complete examination takes only minutes it is central in vital diagnostics.
The disadvantages of CT are the high costs and the small increased risk of adverse health effects from
cancer related to the radiation doses given to the patients 172.
Magnetic resonance imaging is based upon principles of magnetic fields and does not expose the
patients to radiation. It is superior with regard to diagnostics of the soft tissues and organs. Magnetic
resonance imaging is however not displaying fractures as well as CT, and albeit rare, injuries induced
37
during MRI procedures have been reported as the highly magnetic field may cause adverse effects on
implanted devices 173. The accessibility to MRI is fairly good in most developed countries, however the
major disadvantage of MRI is the accessibility, the time needed per procedure and the high costs.
5.2. Fatal road traffic crashes
There is an increasing demand for advanced diagnostic imaging in forensic settings, and CT and MRI
are regarded as useful supplements to the forensic autopsy 168;174-177.
Conventional X-rays inadequately identify discrete osseous lesions in the cervical spine in people killed
after significant trauma, including road traffic crashes 27;30-33;36;46;178-181. Furthermore, in a number of post-
mortem studies, detailed histological examination has shown injuries in the cervical spine that could not
be detected on conventional X-rays or CT 30;46;115;167;175;178;179;182;182-187, and MRI 46;162;167;168;178;187;188.
Despite these findings, a few studies have identified lesions in the cervical spine facet joints using
conventional X-rays 180;189. The soft tissue structures of the facet joints are poorly displayed on MRI
112;115;178. However, a recent publication have identified the cervical spine facet joint folds on a high
energy-field 3.0 Tesla MRI research unit 117 suggesting that with future advancements visualisation of the
facet joint soft tissues may become possible in clinical settings. Overall, there is a scarcity of publications
regarding the lower cervical spine facet joints and the incidence rates of facet fractures, haemarthrosis
and synovial fold injury in these joints based on different diagnostic imaging procedures of people killed
in RTC’s are unknown.
Currently, no large scaled evidence based research has evaluated the validity and reproducibility of
forensic diagnostic imaging procedures and the exact value of diagnostic imaging findings at post-
mortem remains unclear. Although the sensitivity and specificity of advanced diagnostic imaging
modalities (CT and MRI) gradually increase little is known with regard to the inter- and intraobserver
agreement in the field of post mortem imaging. Furthermore, as many such studies have not included
detailed microscopical evaluation of the anatomy visualised on diagnostic imaging, a gold standard (e.g.
microscopical findings) has not been used as reference. Rather, MRI and CT have not been found
adequate as gold standard when it comes to the identification of morphology and pathoanatomical
conditions 42;162;190.
38
5.3. Survivable road traffic crashes
Conventional X-ray studies of the lower cervical spine facet joints of whiplash patients rarely report
somatic lesions, although fractures of the articular columns have been identified in several studies of
traumatised patients, including road traffic crash victims 39-41;191;192. In contrast, conventional X-rays have
been shown to miss large numbers of discrete lesions in the cervical spine of survivors after road traffic
trauma 26;40;164-166;186;192-198. Many of these lesions are likely to be diagnosed on CT 162;164;167;186;198-200
whereas MRI is not expected to have the same sensitivity 42;162;190. Soft tissue lesions are not readily
detected on conventional X-rays as identification is based upon observed distortions of fat lines and
shadow lines. Prevertebral swelling may be present following road traffic crash trauma causing distortion
of the prevertebral shadows which can be identified on conventional X-rays 201-205, although this is much
better visualised on MRI. Another indication of soft tissue injury, and/or osseous injury, is the fanning of
the spinous processes which may be seen on conventional X-rays. This may be caused by injury to the
facet joints, e.g. joint capsule, synovial folds or articular surface which may be identified in some cases
on either conventional X-rays, CT or MRI 39-41;162;164;167;186;191;192;198-200. Changes in the cervical spine
lordosis is a frequent finding in whiplash patients and is thought to be related to factors such as post-
traumatic muscular hypertonicity and segmental articular dysfunction (biomechanical dysfunction)
14;202;206-208, although its exact correlation to trauma has been questioned 209;210. In follow-up studies of
patients suffering from chronic pain after whiplash injury it has been shown that high percentages of
patients develop degenerative changes in the cervical spine in comparison to non-traumatised subjects
211-213, however other studies have not found similar correlations 214.
In several MRI studies of people injured in road traffic crashes, including whiplash trauma, injuries to the
cervical spine have been identified, primarily in the intervertebral discs and ligaments 42-45;190;206-208;215-218.
However, the majority of findings in these studies were degenerative changes rather than acute injuries.
Attempts to correlate MRI findings with the symptoms and the preceding trauma have most often been
inconclusive 45;207;208;215;217;219. In recent years the primary focus for diagnostic imaging has been on the
upper cervical spine where different types of ligamentous injuries have been identified in whiplash
patients 220-222. However, there has been some debate with regard to the validity of these findings
although the body of evidence is mounting 223;224. Nonetheless, this anatomical region is beyond the
purpose of this study.
39
6. Materials and methods
6.1. Materials
Twenty motor vehicle crash fatalities (cases) and 22 non-traumatic decedents (controls) were examined
at medico legal autopsy within 1-5 days (median 3 days) after death and included in this study. The
cases were decedents from motor vehicle crashes in which the decedent had been an occupant of an
involved vehicle and the control subjects had died due to non-traumatic causes. All subjects had to be in
the age range of 20-49 years of either gender. Subjects were excluded if the case record showed
evidence of history of drug and/or alcohol abuse, if there had been any previous injury to the cervical
spine, if there was significant external evidence of cervical spine injury, and if diagnostic imaging
procedures could not be performed within 24 hours of the autopsy. After completion of the inclusion
period, two of the 42 subjects (one case and one control) were excluded due to extensive decomposition
causing generalized tissue damage. The final study group consisted of 40 subjects divided into 19 cases
(15 males (median age 33, range 20-47) and 4 females (median age 27, range 22-45)) and 21 controls
(13 males (median age 35, range 22-49) and 8 females (median age 41, range 27-49)). For the purpose
of this study only the lower cervical spine facet joints from C4-C5, C5-C6, C6-C7 and C7-Th1 were
examined.
The study was approved by the Scientific Ethics Committee, Central Denmark Region, and The Danish
Data Protection Agency.
6.2. Retrieval of specimens
During autopsy the lower cervical spine motions segments from C4 to C7 were retrieved en bloc from
each subject through a conventional “Y”-incision from the front of the neck according to previously
described procedures 225, and stability was restored with a specially designed brace, enabling completion
of the autopsy in such manner that no additional external evidence of the intervention was visible other
than was is normal following post-mortem autopsy. The osteo-cartilaginous specimens consisted of the
lower four cervical vertebral segments (C4-C7) including the vertebral body, pedicles, articular columns,
40
laminae, spinous processes and surrounding muscles without the covering skin. Hence, the facet joints
from C4-C5, C5-C6, C6-C7 and C7-Th1 bilaterally were included. Each specimen was assigned a
reference number (LU-reference), which uniquely identified the subject.
6.3. Diagnostic imaging procedures (see Article I for more details)
After retrieval each specimen was enveloped in a clear plastic bag and placed in a clear plastic box in
which a firm foam rubber structure gave support. The box with the specimen was placed in a clear
airtight envelope. The specimens were examined with the presence of the lead investigator and
consisted of conventional X-rays, computed tomography (CT) and magnetic resonance imaging (MRI).
All the procedures were standard clinical procedures equivalent to what were used on a daily basis in the
diagnostic evaluation of cervical spine trauma patients. The conventional X-ray examination consisted of
anterior-posterior, lateral, bilateral articular pillar and oblique views using an Arcosphere, Arcoma©
equipment. Spiral scanning of the total volume of the specimen was performed on a Phillips© four-slice
MX8000 CT scanner with a slice thickness of 1,3 mm, increments of 0.6 and a matrix of 512x512. Axial,
coronal, saggital and angled reconstructions were performed with bone and soft tissue algorithms.
Magnetic resonance imaging was performed on a General Electrics© 1.5 T Signa scanner using a surface
“temporomandibular” coil. Saggital T1, T2, STIR-sequences, axial T1, T2 and T2*gradient-sequences
were produced of the facet joint structures with the majority of sequences being made with a thickness of
3 mm, spacing 0 and FOV 16x16, and the matrix was 512x512 on the saggital sequences and 256x256
on the remaining.
Results from the first, second and third neuroradiological examinations (see below) were entered directly
onto response sheets, produced for the purpose of this study, independently by either observer. From
there direct entry into Excel, Microsoft© spreadsheets were possible.
At all times were the staff , including the participating radiologists, blinded with regard to the descriptive
characteristics of the subject examined and the lead investigator did not influence the interpretations or
conclusions made by the radiologists.
6.3.1. The first examination of the radiological images
In the first evaluation of radiological images all images from conventional X-rays, CT and MRI were
scored independently by two experienced neuroradiologists, with regard to general facet fractures and
41
haemarthrosis/excess fluid in the facet joints. No training or coaching was given prior to the first
evaluation and the scoring was based on routine clinical interpretation.
6.3.2. The second examination of the radiological images
A second evaluation was performed by both observers together during which consensus agreement was
obtained with regard to fractures on all imaging modalities, and haemarthrosis/excess fluid in a facet joint
on conventional X-rays and CT-scanning only.
6.3.3. The third examination of the radiological images
A third evaluation of the MR-images was performed by both observers independently and blinded with
regard to haemarthrosis/excess fluid in the facet joints only. Prior to the third evaluation the observers
defined consensus regarding scoring this variable. Hence, the variable was defined as a joint showing
focally increased signal, with signal differences between adjacent joints on any sequence or relatively
increased signals in all joints.
6.4. Histolaboratory procedures (see Article II & III for more details)
Immediately after the neuroradiological examinations the specimens were embedded in five litres 70 %
ethanol. After two weeks the specimens were divided by hemisection in the median plane and re-
embedded in 70 % ethanol for an additional three weeks, followed by one week in 96 % ethanol under
vacuum conditions fixation and a final week in 99 % ethanol. The hemisection was performed using an
industrial bandsaw and improved the efficiency of the alcohol fixation (Figure 6.1). After fixation each
specimen was embedded in liquid methylmethacrylate (MMA) and dibutylphtalate (a softener) in a
refrigerator for six weeks under continuous supervision, after which percadox (a catalyst) was added to
complete polymerisation and hardening into a plastic bloc 226-228. The hardened plastic bloc contained
one side of the un-decalcified specimen. At no time was the specimens frozen or decalcified.
An independent registrar who was blinded with regard to the descriptive characteristics of each subject
assigned each pair of plastic blocs with a two-digit reference number (k-reference subject number) as
well as a side label identifying the left and right side allowing identification of each unique subject. The
registrar was in charge of a codebook consisting of the reference number (LU-reference), originally
assigned by the lead investigator, prior to neuroradiological examination, and the corresponding k-
42
Figure 6.1 Illustration of a cervical spine specimen
The lower four cervical spine segments (corpora C4 to C7) viewed from the posterior (A). Illustration of
hemisectioning of the cervical spine sample approximately through the midline (median) with crude estimated
location of the individual spinal segments (B).
43
reference number. The codebook was disclosed to the participating physicians only at the time when all
evaluations had been completed. Hence, adequate blinding was obtained for all consequent evaluations
of the material by the lead investigator and the senior pathologists.
In addition to the k-reference and the LU-number a case number uniquely identified each specific facet.
The case number consisted of a 6-digit number made according to the order of appearance; two digits
from the k-reference number (legal values: 12-54), one digit from the side (legal values: 1 left, 2 right),
one digit from the slice (legal values: 1-9), one digit from the segment (legal values: 1 (Th1), 4-7 C4-C7))
and one digit from the facet orientation (legal values: 1 superior, 2 inferior). For example, case 422562
was equivalent to the subject with k-reference 42, right side, slice 5, segment C6 and the inferior facet.
6.4.1. Production of the 3-mm thick anatomical slices
From a random medial starting point, each plastic embedded hemisected cervical spine was sawed by
serial sectioning, into continuous approximately 3-mm thick parasaggital slices using a precision guided
bandsaw (Femi©, Bologna, Italy) (Figure 6.2). The guiding equipment ensured comparable thicknesses of
the slices with an additional tissue loss of approximately 1 mm per slice due to sawing. A total of 280 3-
mm thick slices were produced.
Each slice was given consecutive numbers with the most medial slice being numbered one and the most
lateral slice receiving the highest number, and a label containing the slice number, side and case
identification was fitted on the lateral aspect of the slice. The slices were cleaned and placed in a
photographic documentation bay where digital photographs were made in overview using a “μ [mju:] 400
digital”, Olympus© camera. These photographs were printed and used as reference material for the
subsequent stereomicroscopical examination of the 3-mm thick slices.
Detailed photographs of each facet joint were made using a Camedia C5050, Olympus© through a
stereomicroscope (SZX9, Olympus© with a 0.5X optical) with a direct capture function storing the images
directly in a database (DP-Soft, Olympus©). However, these photographs were not used in the present
study.
6.4.2. Examination of the 3-mm thick anatomical slices
Each 3-mm thick slice was examined with stereomicroscopy by one of two experienced pathologists and
scored with reference to injury of the facet cartilage and/or bone, bleeding in a joint, the presence of
44
Figure 6.2 Illustration of the sawing of 3-mm thick slices from a cervical spine specimen
The hemisected cervical spine viewed from the posterior with a black frame illustrating the line of parasaggital
sectioning for a 3-mm thick slice (A). The parasaggital 3-mm thick slice from the medial part of the facet joint is
viewed from the side visualising the articular column with the facet joints from C4-5, C5-6, C6-7 and C7-Th1 (B).
45
synovial folds and injury to the synovial folds. The findings were recorded on a reply sheet produced for
the purpose and entered into an Excel sheet, Microsoft©.
Furthermore, all 3-mm thick slices were documented with direct radiography using a faxitron medical
imaging device, Hewlett-Packard©. However, these images have not been evaluated in the present
study.
6.4.3. Production of the 10 μm thick histological sections
All the 3-mm thick slices containing facet joints were re-embedded in MMA. After polymerisation a
cleaning layer was removed from the surface using a heavy-duty microtome (SM 2500, Leica©) after
which two consecutive histological sections of 10 μm thickness were produced from each bloc. All the
histological sections were stained with Masson-Goldner trichrome, and mounted un-deplastified on glass
slides. The Masson-Goldner trichrome was chosen as it is particularly useful when staining alcohol
fixated plastic embedded undecalcified osteo-cartilaginous specimens 226-228. In selected cases additional
sections were produced and stained with Safranin O fast-green, haematoxylin-eosin and/or touluidine
blue.
6.4.4. Examination of the 10 μm thick histological sections
A total of 636 unique facets were available for examination as 39 subjects each had 16 unique facets
and the remaining one subject had only 12 due to a bloc vertebra with partial fusion of the facet joints
bilaterally of one motion segment. A total of 1830 unique observations (~46 observations per subject)
were made each containing information regarding morphological and histomorphometric variables (Table
6.1).
The morphological variables were examined with light microscopy using a BX51, Olympus© microscope
and relevant images were photographically documented through a light microscope with a digital camera
(Camedia C5050, Olympus© or D70s, Nikon©). The morphological variables included; cartilage flaking,
cartilage fissures (mild, moderate and severe), cartilage split, vascular invasion, osteophytes, presence
and integrity of the anterior and posterior fold, facet fractures, osteochondral fissures with or without
bleeding, bleeding in the joint space (haemarthrosis), bleeding in the folds (anterior, posterior or both
simultaneously) and bleeding in the underlying bone (Table 6.1).
The histomorphometric variables (Table 6.1) were obtained by measurements of projected images from
46
Variables Description Measurement/scoring
Morphological
flaking Flaking is defined as superficial fibrillation (discontinuity or cracks of the superficial matrix) anywhere on the surface
of the hyaline articular cartilage
no, yes, don’t know and missing
split Split is defined as one or more horizontal (0-60o to the articular cartilage surface) matrix separations of any size of the
hyaline cartilage anywhere within the calcified cartilage
no, yes, don’t know and missing
fissure A fissure is defined as one or more vertical fissures (60-90o to the articular cartilage surface) anywhere within the
hyaline cartilage, and the most extensive fissure as defined as the highest percentage of the total non-calcified
hyaline cartilage thickness at the line of measurement is scored
no, more than 0% and less than 50%, 50% to less
than 100%, 100%, don’t know and missing
fracture A fracture is defined as a separation/discontinuity of osseous components (cortex, spongious and subchondral bone)
with the presence of erythrocytes in and around the lesion site
no, yes, don’t know and missing
osteochondral fissure An osteochondral fissure is defined as a continuous line of separation of tissue components affecting both the
subchondral bone and the adjacent cartilage. This is furthermore evaluated for the presence of blood in the line of
separation
no, present without blood, present with blood, don’t
know and missing
vascular invasion Vascular invasion is defined as a blood vessel, or structure resembling a vascular structure in which erythrocytes are
present, that indents or penetrates the tidemark at the base of hyaline cartilage
no, yes, don’t know and missing
osteophytes An osteophyte is defined as a prominent outgrowth of bony structures at the periphery of the joint margins in close
proximity to the anterior or posterior cartilage borders
no, yes, don’t know and missing
blood in the joint space Blood in the joint space is defined as the presence of erythrocytes within the confines of the joint spaces. Is there
blood in the joint space not including the synovial fold area? Defined as the presence of significant erythrocytes in the
joint space (intra-articular)
no, yes, don’t know and missing
blood in the synovial folds Blood in the synovial fold is defined as presence of extra vascular erythrocytes within any of the anterior or posterior
synovial folds
no, yes but anterior fold only, yes but posterior fold
only, yes and both folds, don’t know and missing
blood in the bone Blood in the bone is identified as significant localised extra vascular bleeding in either a fracture site or excessive
blood in the marrow space of the bone
no, yes, don’t know and missing
presence of the anterior &
posterior fold The presence of tissue that exhibits the structure and location of an anterior or posterior synovial fold respectively no, yes and intact, yes and disrupted, don’t know and
missing
Histomorphometric
cartilage length The linear distance of the cartilage covering of each facet, measured on all 10μm thick sections. The distance is
measured in millimetres from the most anterior to most posterior aspect of the cartilage. The measure points of the
cartilage borders are determined by the observer as the estimated point where hyaline cartilage no longer covers the
articular surface
The length is measured on the projected image using
1x magnification, 1 mm equals 19.25 mm projected
on the table. Not measurable and missing values are
recorded
the anterior & posterior
fold overlap The anterior and posterior fold overlaps of the hyaline cartilage are measured. A line perpendicular to and through
the cartilage length line at the anterior and posterior endpoints form the basis. From this basis line the maximal length
of the respective folds extending towards the joint centre is recorded in millimetres. If the length of the fold is more
than the total measured length of the cartilage, then it is scored “100%” (if the overlap can confidently be ascribed to
the respective fold alone) or “complete” (if the overlap is a combined overlap of the anterior and posterior fold)
The overlap is measured on the projected image by
4x magnification, 1 mm equals 77.00 mm projected
on the table. Complete and 100% overlap, not
measurable and missing values are recorded
joint-tidemark The joint-tidemark is the distance measured from the joint space surface of the articular hyaline cartilage to the
tidemark separating the hyaline from the calcified cartilage. The tidemark is identified as the line dividing the green
and red staining on the Masson Goldner-Trichrome staining in the part of the deep cartilage. The measurement is
performed along a gridline that is perpendicular to the cartilage length line. The variable is recorded at maximally 5
intersections through each facet
The recorded value is measured in millimetres on the
projected image, which is at 4x magnification, 1 mm
equals 77.00 mm projected on the table. Not
measurable and missing values are recorded
tidemark-osteochondral The tidemark-osteochondral is the distance measured from the tidemark to the osteochondral junction. The
osteochondral junction is defined as the border between the light green and darker green stained areas on the
Goldner Trichrome staining. The measurement is performed along a gridline that is perpendicular to the cartilage
length line. The variable is recorded at maximally 5 intersections through each facet
The recorded value is measured in millimetres on the
projected image, which is at 4x magnification, 1 mm
equals 77.00 mm projected on the table. Not
measurable and missing values are recorded
osteochondral-bone The osteochondral-bone is the distance measured from the osteochondral junction to the bony edge. The bony edge
is defined as the first coming area devoid of bone with a minimum size of five millimetres in any length between bone
borders. The measurement is performed along a gridline that is perpendicular to the cartilage length line. The
variable is recorded at maximally 5 intersections through each facet
The recorded value is measured in millimetres on the
projected image, which is at 4x magnification, 1 mm
equals 77.00 mm projected on the table. Not
measurable and missing values are recorded
Table 6.1 Description of the morphological and histomorphometric variables
47
a BH2 Olympus© microscope with objectives x1 or x4, through a projection arm to a measuring table with
a final magnification factor on the table of 19.25 or 77.00 respectively (Figure 6.3).
These variables included information regarding; the hyaline cartilage length, the degree of overlap of the
anterior and posterior fold in relation to the underlying hyaline cartilage covering of the facet (Figure 6.4),
and the thicknesses of the hyaline cartilage, the calcified cartilage and the subchondral bone (Figure
6.5). The measurements were performed with a metallic ruler of the projected images and the measured
values were recorded. During statistical analysis these values were transformed by the known
magnification factor in order to correct for the effect of the magnification of the projected image (Table
6.1).
In order to randomise the recording sites for the thickness of the hyaline cartilage, calcified cartilage and
the subchondral bone the starting point for each observation was always anteriorly. The location was
determined by a random value produced in Excel, Microsoft© whereby the consequent recordings could
be made from the selected point moving from anterior to posterior with an absolute interval of 3.5 mm (on
the original object) between the lines of each measurement.
6.4.5. Handling of data from the 10 μm thick histological sections
The results from the examination of the 10μm thick histological sections were entered directly onto a
specially designed A-3 sheet containing all variables. After completed examination of all the histological
sections the data were entered twice into Epidata© vs. 3.02, a freeware software program for data entry
and documentation 229, by two independent persons in two separate files. Each person entered a total of
114.028 unique entries using the Epidata© data entry software. By having two separate files comparison
of the entries could be performed using an integrated validation function in Epidata©. Furthermore,
double entry of the case identifying variables (k-reference and case number) ensured entry of data
relevant to each unique facet. After the complete entry, comparison was performed on selected key fields
and missing observations were identified and corrected producing a 100 % response rate for all variables
in the dataset. The Epidata© function “validation of duplicate files” allowed identification and correction of
discrepancies between the two data files producing the final data set. This identified 34 field errors
(inconsistencies) in 20 observations of the morphological data (equivalent to error in 0.07% of the 51116
field registrations), and 153 field errors (inconsistencies) in 112 observations of the histomorphometric
data (equivalent to error in 0.24% of the 62912 field registrations). All field errors were corrected in both
48
Figure 6.3 Setup for histomorphometric measurements
The projection arm mounted on the BH2, Olympus© microscope through which the images are projected onto the
table. The magnification factor for the projected image on the table was measured for each objective used on the
revolver, i.e. objective x1 resulted in a magnification factor of 19.25 whereas objective 4x resulted in a
magnification factor of 77.00.
49
Figure 6.4 Histomorphometric quantitative measurements
Histomorphometric measurements of the cartilage length (a), and the anterior fold (b) and the posterior fold (c)
overlap of the underlying facet.
50
Figure 6.5 Random location of histomorphometric measurements
A “birdseye” view of the facet cartilage of a superior articular facet with the parallel lines resembling the
parasaggital 3-mm thick slices (A). A parasaggital histological section, equivalent to one of the 3-mm thick slices,
through the articular facet with the localisation of the measurement lines (1-5) through the cartilage and bone
determined at random prior to the first reading (B).
51
independent data files and following repeated comparison confirmation of complete agreement between
the files was obtained.
6.4.6. Evaluation of the inter- and intraobserver agreement of the morphological findings
For the purpose of interobserver agreement testing 10 μm thick sections from four randomly chosen
facets from each subject were used. Hence, a total of 160 facets were eligible for this evaluation,
however only 159 unique facets were evaluated as the remaining one facet did not contain articular
structures. All facets were examined independently by two examiners (the lead investigator and a senior
pathologist) who were blinded with regard to the descriptive characteristics of the subjects. Only the
morphological variables were tested in this manner. The results from each observer were entered into an
Excel, Microsoft© spreadsheet. Approximately six months after the first examination of the 160 randomly
chosen facets, the lead investigator conducted a repeated examination of the same facets with the
purpose of intraobserver agreement testing. Prior to this, two independent laboratory assistant had
assigned the facets with new running numbers whereby blinding and randomisation of the facets was
obtained. The results from the repeated examination were entered into an Excel, Microsoft© spreadsheet
and compared with the results from the first examination.
6.5. Police records and information from the medico-legal autopsy
Data from each medico-legal autopsy were obtained by a forensic pathologist who recorded pathological
conditions and concluded upon the diagnosis. Included in the information available to the forensic
pathologist were data from the law enforcement (police records). These observations were kept in the
classified archives of the Institute of Forensic Medicine. Access to the archive was available on-site only
and the discretion of personal data was maintained when obtaining relevant information, which was
copied and entered into an Excel, Microsoft© spreadsheet.
6.6. Statistical analysis
The association of groups was tested with Fisher’s exact test and Chi-squared test. Measurements of
agreement between the same and different observers, as well as between different diagnostic methods
were tested with kappa ( ) statistics 230. The data were analysed with a linear regression model
assuming linear association, normal distribution and independence (homoskedasticity) of residuals. The
52
regression model used for the morphological data examined for correlation between gender, age and
trauma versus no trauma and a reference person was defined as a 35 years old male who had been
killed in a road traffic crash. The regression model used for the histomorphometric data examined for
correlation between gender, age, trauma versus no trauma, side and facet per segment and a reference
person (level) was defined as the left C4 inferior facet of a 35 years old male who had been killed in a
road traffic crash. The potential effect of interaction was not tested due to the limited number of subjects
(n=40). Results including 95 % confidence intervals were presented in brackets, e.g. 75 μm [69-80]. In all
statistical tests the significance level was p < 0.05. All statistical analyses were performed using Stata© 9
(StataCorp LP, College Station, USA).
53
7. Summary of results
7.1. Diagnostic imaging findings (Paper I)
Initial examination of all neuroradiological images obtained of the lower cervical spine facet joints,
including conventional X-rays, CT and MRI, was performed by two senior radiologists in a blinded and
independent fashion with regard to articular facet fracture and haemarthrosis/excess fluid in a joint. This
revealed that CT was the most sensitive for the detection of facet fractures, followed by MRI and
conventional X-rays. Overall, agreement was “substantial” between the observers with kappa scores
ranging from 0.66–0.79 [0.37-1.09] (range [95 % confidence intervals]), p < 0.001. Based on consensus
agreement, facet fractures were present on neuroradiology in four trauma cases (4/19) only. Computed
tomography was the only modality capable of identifying all cases with facet fractures, where MRI
identified three and conventional X-rays one case with facet fractures. The agreement between the
observers initial (first) evaluation and the consensus (second) evaluation was substantial to almost
perfect for both observers with regard to facet fractures with kappa scores ranging from 0.66-1.00 [0.37-
1.31], p < 0.001 (unpublished data).
On neither conventional X-rays nor CT was haemarthrosis/excess fluid in a joint observed. There was
poor agreement between observers in a third evaluation on MRI only of haemarthrosis/excess fluid in a
joint in which 38 subjects (38/40) were scored positive by one or both observers ( = 0.31 [0.00-0.62], p <
0.05) with no statistically significant correlation to trauma.
Comparing the initial MR findings (first evaluation) to the third evaluation findings (MRI only) with regard
to haemarthrosis/excess fluid in a joint both observers obtained poor agreement, with one scoring ( =
0.04 [-0.05-0.13], p = 0.183) and the other scoring ( = 0.17 [0.00-0.34], p < 0.05) (unpublished data).
The findings on microscopy of haemarthrosis and bleeding in the synovial folds could not be confirmed
with any diagnostic imaging procedure (Figure 7.1).
In comparison to microscopical evaluation of the 10 μm thick sections only three subjects with facet
fractures were identified by both microscopy and CT (Figure 7.2) (Table 7.1) (Appendix 1). The fourth
facet fracture identified on CT and MRI was not identified on microscopy. A discrete fifth facet fracture at
54
Figure 7.1 Discrete injuries to the cervical spine facet joint soft tissue structures
Overview of an injured joint (A). The disrupted synovial fold with bleeding (a), and haemarthrosis in the joint
space (b) was only identified on microscopical examination of the 10 μm thick section (B), original magnification
x1.25 and x4. Stained with Masson-Goldner trichrome.
55
Figure 7.2 Cervical spine facet fracture in a motor vehicle crash fatality
The fracture through the superior facet of C6 was identified on both microscopical examination of the 10 μm thick
section, original magnification x1, Masson-Goldner trichrome (left) and computed tomography 3-D reconstructed
image (right).
56
Subject # 10 μm histology CT consensus 22 (case) C5 right IAP fracture -
25 (case)
C5 left IAP fracture C6 left SAP fracture C6 left IAP fracture C7 left SAP fracture C6 right SAP fracture
-C6 left SAP fracture ---
39 (case) Th1 left SAP fracture -C5 right IAP fracture
Th1 left SAP fracture C7 left IAP fracture -
53 (case) C7 left IAP fracture C6 right IAP fracture C7 right SAP fracture
-C6 right IAP fracture C7 right SAP fracture
24 (case) - Th1 left SAP fracture
The total number of unique facets is 636 among the 40 subjects SAP: superior articular process IAP: inferior articular process
Table 7.1 Subjects with unique facet fractures on either histology or CT consensus
57
the osteochondral junction was identified on microscopy only. There was “substantial” agreement
between the CT consensus findings and the microscopical findings with regard to identifying subjects
with facet fractures, and “moderate” agreement when identifying unique facet fractures. Computed
tomography had a sensitivity of 0.67 (95 % confidence interval: 0.29-1.04) and a specificity of 0.99 (95 %
confidence interval: 0.98-1.00) with regard to detecting facet fractures identified on the microscopy.
Key points Paper I CT was the most sensitive imaging modality with regard to detection of facet fractures
less than ½ of all unique facet fractures were identified on diagnostic imaging procedures
observers generally agreed on the presence of facet fractures on all imaging modalities
haemarthrosis could not be reliably identified on any diagnostic imaging procedure
58
7.2. Pathological findings (Paper II)
Stereomicroscopy of 3-mm thick slices and microscopical examination of 10 μm thick histological
sections from the lower cervical spine facet joints of motor vehicle crash victims and controls was
performed. Using stereomicroscopy damage to the facet cartilage and/or bone and haemarthrosis was
identified in a several subjects, however there was no significant correlation between exposure to trauma
and the findings, and the folds were poorly identifiable and no injuries were detected in the folds. In
contrast to the stereomicroscopy, light microscopy identified discrete injuries to the lower cervical spine
facet joints in large numbers among the victims of fatal motor vehicles crashes (Table 7.2). Light
microscopy identified four trauma cases with facet fractures (Figure 7.3) and three had osteochondral
fissures with bleeding that corresponded significantly with trauma, p < 0.05 and p < 0.01, respectively.
Soft tissue lesions were particularly common, with bleeding in any fold being the most frequent finding,
and simultaneous bleeding in both folds at any one segment was significantly correlated to trauma (p <
0.05) and to the presence of a fracture (p < 0.01). Haemarthrosis was identified in nine trauma cases
(Figure 7.4) and correlated significantly with trauma (p < 0.01), as well as with the presence of a fracture
(p < 0.05) and bleeding in both synovial folds at the same segment (p < 0.01). Disruption of the synovial
folds was common in the whole study population, but when the number of disrupted folds per subject
were calculated this showed significant correlation with trauma (p < 0.01). There was no statistically
significant correlation between the stereomicroscopy and microscopical findings concerning damages to
the facet cartilage and/or bone or the synovial folds.
Key points Paper II facet fractures, haemarthrosis and bleeding in folds were common after fatal traffic crashes
there was significant correlation between pathology and trauma
light microscopy was superior to stereomicroscopy in the evaluation of pathology
conventional autopsy procedures did not reveal any of the injuries to the facet joints
Subj
ect
Age
Gen
der
Frac
ture
of a
fa
cet
OC
F w
ith b
lood
(0
-16
face
t)O
CF
with
out
bloo
d
(0-1
6 fa
cet)
Blo
od in
any
jo
int s
pace
Blo
od in
any
fo
ld*
Blo
od in
bot
h fo
lds±
Ant
erio
r fol
d di
srup
ted
(0-8
join
ts)
Post
erio
r fol
d di
srup
ted
(0-8
join
ts)
Blo
od in
the
unde
rlyin
g bo
ne
2621
MN
o0
10N
oN
oN
o3
7Ye
s
2422
FN
o0
10N
oYe
sN
o0
1Ye
s
3533
MN
o0
16N
oN
oN
o1
4N
o
1420
MN
o0
5Ye
sYe
sN
o3
6Ye
s
2029
MN
o0
9N
oN
oN
o0
0N
o
2536
MYe
s4
7Ye
sYe
sYe
s8
3Ye
s
4229
MN
o0
6N
oN
oN
o0
1Ye
s
4723
FN
o0
10Ye
sYe
sYe
s3
5Ye
s
2131
FN
o0
6N
oYe
sno
76
Yes
1334
MN
o0
6N
oYe
sN
o2
8Ye
s
1745
FN
o0
8N
oN
oN
o0
2Ye
s
1935
MN
o0
9Ye
sN
oN
o1
4Ye
s
2220
MYe
s1
13Ye
sYe
sYe
s8
7Ye
s
3629
MN
o0
10Ye
sYe
sN
o5
7Ye
s
4637
MN
o0
10Ye
sYe
sN
o3
2N
o
5331
MYe
s0
13N
oN
oN
o3
7N
o
3941
MYe
s1
15Ye
sYe
sYe
s6
5Ye
s
3447
MN
o0
10Ye
sYe
sYe
s1
3Ye
s
2838
MN
o0
8N
oN
oN
o2
5Ye
s
19 c
ases
46
181
(59.
2%)
911
556
(37.
3%‡)
83 (5
5.3%
‡)15
(p<0
.05)
(p<0
.01)
(n.s
.)(p
<0.0
1)(n
.s.)
(p<0
.05)
(p<0
.01)
(p<0
.01)
(n.s
.)
‡ p
erce
ntag
e of
all
fold
s in
the
grou
ps (t
wo
fold
s ar
e no
n-ex
istin
g du
e to
a b
loc
verte
brae
in o
ne tr
aum
a ca
se)
OC
F: o
steo
chon
dral
fiss
ure
n.s.
: not
sta
tistic
ally
sig
nific
ant
* bl
eedi
ng in
the
ante
rior a
nd/o
r pos
terio
r fol
ds a
t any
seg
men
t per
sub
ject
± s
imul
tane
ous
blee
ding
in b
oth
fold
s at
any
seg
men
t per
sub
ject
Gen
der:
M (m
ale)
, F (f
emal
e)
Tabl
e 7.
2 H
isto
path
olog
ical
find
ings
in th
e ro
ad tr
affic
cra
sh fa
talit
ies
59
Figure 7.3 Injuries to the cervical spine facet joint in a motor vehicle crash fatality
Large overview of the anterior part of a facet joint, original magnification x1.25 (A). Close-ups of an osteo-
chondral fracture at the superior articular facet (B) and widespread bleeding in the anterior synovial fold and in
the joint space, original magnification x4 (C). Stained with Masson Goldner-Trichrome.
60
61
Figure 7.4 Haemarthrosis in a cervical spine facet joint in a fatal motor vehicle crash victim
Large overview of the joint with the inferior and superior facets, original magnification x1.25 (A). The close-up
illustrates bleeding in the joint space with an intact synovial fold, original magnification x4 (B). Stained with
Masson Goldner-Trichrome.
62
7.3. Anatomical and age-related findings (Paper III)
Microscopy of all histological sections containing articular facets (n=636) was performed with regard to
morphological and histomorphometric variables providing 1830 unique observations in total. Inter- and
intraobserver agreement was tested on four randomly selected facets from each subject with regard to
selected morphological variables. Significant age-, gender and trauma related changes in the bone,
cartilage, and soft tissues were observed. Flaking of the cartilage surface was the commonest finding in
more than half of the facets, followed by split and fissures (Figure 7.5). Osteophytes were only present in
approximately 4 % of the facets at the age of 35 years. Females were less affected by flaking, split and
fissures than males. The length of the cartilage in males was approximately 11.4 mm, whereas in
females it was significantly shorter (by approximately 1.3 mm) and the articular facets appeared to be
completely covered with cartilage without free bony edges (“cartilage gaps”) in far the majority of cases.
Ageing was significantly related to an increase in the number of facets with flaking, split and osteophytes.
The subchondral bone thickness increased significantly with increasing age equivalent to an increase of
approximately 10 % per decade. The presence of fissures did not correlate significantly with age. In the
trauma group there were significantly more disrupted anterior and posterior folds, and more articular
facets with cartilage split. However, fissures and flaking did not correlate to trauma. In the reference
person (a 35 years old male) the anterior and posterior fold overlap of the underlying cartilage was
approximately 16 % and did not differ between genders or with ageing. Furthermore, synovial folds were
consistently identified anteriorly and posteriorly in all but one facet joint, and in some histological section
the folds completely filled the joint space (Figure 7.6). Significant systematic differences were observed
between individual cervical spine segments from C4 to Th1, although none of these segmental variations
appeared to be linear. The thicknesses of the hyaline cartilage, the calcified cartilage, the total articular
cartilage and the calcified cartilage percentage of the total articular cartilage were not different between
genders and showed no correlation with ageing. There was overall moderate interobserver agreement
and good intraobserver agreement for the description of the morphological variables. The most important
morphological and histomorphometric findings are presented in Table 7.3 and Table 7.4 respectively.
63
Figure 7.5 The morphological variables
Vertical fissures are present in the deep and middle part of the cartilage, original magnification x4 (A).
Widespread superficial flaking/fibrillation of the cartilage, original magnification x10 (B). Large horizontal split
through the middle part of the hyaline cartilage, original magnification x4 (C). Example of vascular invasion of the
tidemark, original magnification x10 (D). All stained with Masson-Goldner trichrome.
64
Figure 7.6 Complete covering of the articular surface by the synovial folds
In this parasaggital section through the lateral part of a cervical spine facet joint there is complete covering of the
articular surfaces with a synovial fold, with the posterior fold (A) and anterior fold (B) illustrated in close-up,
original magnification x1.25 and x4, Masson-Goldner trichrome.
Estim
ate
95%
CI
Estim
ate
95%
CI
p-va
lue
Estim
ate
95%
CI
p-va
lue
Estim
ate
95%
CI
p-va
lue
Flak
ing
(%)
75[6
7-83
]-1
8[-2
9-(-7
)]<0
.01
13[7
-20]
<0.0
01-4
[-15-
(7)]
0.46
0S
plit
(%)
72[6
5-78
]-1
8[-2
7-(-9
)]<0
.001
8[3
-13]
<0.0
1-1
0[-1
8-(-1
)]<0
.05
Any
fiss
ure
(%)
58[4
9-67
]-1
3[-2
6-(-1
)]<0
.05
0[-7
-7]
0.98
5-2
[-14-
10]
0.73
1A
nter
ior f
old
disr
uptio
n (%
)16
[8-2
3]2
[-8-1
3]0.
655
-1[-7
-6]
0.87
9-1
1[-2
1-(-1
)]<0
.05
Pos
terio
r fol
d di
srup
tion
(%)
33[2
3-43
]-8
[-22-
5]0.
210
-10
[-18-
(-3)]
<0.0
5-1
5[-2
7-(-2
)]<0
.05
Ref
eren
ce p
erso
n: 3
5 ye
ars
old
mal
e ki
lled
in a
road
traf
fic c
rash
Varia
ble
Exam
ple:
a 3
5 ye
ars
old
fem
ale
is p
redi
cted
to h
ave
flaki
ng in
app
roxi
mat
ely
57%
, i.e
. 18%
few
er fa
cets
than
mal
es (P
<0.0
1). T
here
is a
n ag
e-re
late
d in
crea
se in
the
num
ber o
f fac
et w
ith fl
akin
g eq
uiva
lent
to
13%
per
dec
ade
(p<0
.001
) and
no
sign
ifica
nt c
orre
latio
n w
ith tr
aum
a (p
=0.4
60)
Incr
ease
per
10
year
s
AGE
Con
trol v
s. C
ase
CAS
E/C
ON
TRO
LG
END
ER
Fem
ales
vs.
Mal
esR
efer
ence
per
son
Tabl
e 7.
3 M
orph
olog
ical
find
ings
of t
he lo
wer
cer
vica
l spi
ne a
rtic
ular
face
t
65
66
Estim
ate
95%
CI
Estim
ate
95%
CI
p-va
lue
Estim
ate
95%
CI
p-va
lue
Estim
ate
95%
CI
p-va
lue
Hya
line
carti
lage
thic
knes
s (m
m)
0.72
[0.6
7-0.
77]
-0.0
5[-0
.11-
0.02
]0.
152
0.00
[-0.0
4-0.
04]
0.96
60.
04[-0
.02-
0.10
]0.
180
Cal
cifie
d ca
rtila
ge th
ickn
ess
(μm
)79
[68-
90]
5[-8
-17]
0.47
17
[-1-1
4]0.
080
0[-1
2-12
]0.
972
Sub
chon
dral
bon
e th
ickn
ess
(mm
)0.
35[0
.31-
0.39
]0.
03[-0
.02-
0.07
]0.
229
0.04
[0.0
1-0.
06]
<0.0
10.
00[-0
.04-
0.04
]0.
852
Thic
knes
s of
the
tota
l arti
cula
r car
tilag
e (m
m)
0.80
[0.7
5-0.
85]
-0.0
4[-0
.10-
0.02
]0.
207
0.01
[-0.0
3-0.
04]
0.70
80.
04[-0
.02-
0.10
]0.
184
Max
imum
car
tilag
e le
ngth
(mm
)11
.35
[10.
66-1
2.04
]-1
.33
[-2.1
9-(-0
.46)
]<0
.01
-0.2
0[-0
.70-
0.30
]0.
435
0.54
[-0.2
9-1.
37]
0.20
4C
alci
fied
carti
lage
of t
otal
arti
cula
r car
tilag
e th
ickn
ess
(%)
10[9
-12]
1[-1
-3]
0.17
71
[0-2
]0.
123
-1[-2
-1]
0.48
9A
nter
ior f
old
over
lap
(%)
16[1
1-21
]0
[-6-6
]0.
974
1[-2
-4]
0.62
25
[0-1
1]0.
055
Pos
terio
r fol
d ov
erla
p (%
)17
[13-
21]
2[-2
-7]
0.31
41
[-2-4
]0.
460
3[-2
-7]
0.24
5
Ref
eren
ce le
vel:
the
C4
infe
rior f
acet
of a
35
year
s ol
d m
ale
kille
d in
a ro
ad tr
affic
cra
sh
Varia
ble
Exam
ple:
a 3
5 ye
ars
old
fem
ale
has
a hy
alin
e ca
rtila
ge th
ickn
ess
equi
vale
nt to
that
of m
ales
(0.0
5 m
m th
inne
r, p=
0.15
2). T
here
are
no
age-
rela
ted
diffe
renc
es w
ith re
gard
to th
e th
ickn
ess
(p=0
.966
) and
ther
e is
no
sign
ifica
nt c
orre
latio
n w
ith e
xpos
ure
to
traum
a (p
=0.1
80).
Incr
ease
per
10
year
s
AGE
Con
trol v
s. C
ase
CAS
E/C
ON
TRO
LG
END
ER
Fem
ales
vs.
Mal
esR
efer
ence
leve
l
Tabl
e 7.
4 H
isto
mor
phom
etric
find
ings
of t
he lo
wer
cer
vica
l spi
ne a
rtic
ular
face
t
Key points Paper III males are more affected by degenerative changes in the cervical spine facets than females
degenerative changes in the articular cartilage are common from a young age
two synovial folds are consistently present in the cervical spine facet joints
pathological lesions are produced in facet cartilage and soft tissues after road traffic crashes
67
68
7.4. Other findings
7.4.1. Inter- and intraobserver agreement
All morphological variables were evaluated for the purpose of inter- and intraobserver agreement testing
using the 10 μm thick sections from four randomly chosen facets per subject. Based on the random
number generator in Excel, Microscoft© random slices, segments and orientations of two facets from
each side from each subject were selected. Some of the findings have been presented in Paper III,
however, for the purpose of clarity all observer scores are tabulated here (Table 7.5).
The agreement between the two observers was “moderate” in four variables (fissures, flaking, posterior
fold disruption and haemarthrosis) with kappa scores between 0.41 and 0.60 (p < 0.001). In four
variables (bleeding in folds, split, vascular invasion, and facet fracture) the agreement was “fair” with
kappa scores between 0.21 and 0.40 (p < 0.001). The agreement was “slight” with kappa scores
between 0 and 0.20 for the variables blood in the subchondral bone, osteochondral fissure (p < 0.05),
and anterior fold disruption (p = 0.156). There was “poor” agreement with a kappa score below 0 (p =
0.688) for the presence of osteophytes 230. As expected, the intraobserver agreement was better than the
interobserver agreement. Where the interobserver agreement generally was fair to moderate, the
intraobserver agreement was generally substantial.
7.4.2. Police records
For all subjects the police records were reviewed in detail with regard to information pertaining to the
circumstances of death and for all trauma cases data were retrieved concerning the mechanism of
trauma. In eighteen of the trauma cases (18/19 cases) the decedent was the driver of a passenger car.
The crash occurred mostly on dry roads, in darkness, with the involved vehicle driving straight ahead on
a main road without any road lightning. The collision was most often a frontal collision involving more
than one party. For practical purposes only the most important data are presented in Appendix 2.
Toxicological evaluation revealed a blood alcohol concentration (BAC) > 0.8 mg/ml in eight subjects
(5/19 cases and 3/20 controls tested), with four drivers (4/18 drivers) killed in a motor vehicle crash being
under the influence of alcohol (BAC > 0.8 mg/ml in three cases and alcohol concentration in the vitreous
humor of 2.4 mg/ml in one case). Medication was found in four subjects (3/9 cases tested and 1/10
controls tested) and narcotics were found in three subjects (1/9 cases tested and 2/10 controls tested).
The toxicological data were presented in part in Paper II and are presented in Appendix 3.
69
Simple agreement Kappa p-value
Simple agreement Kappa p-value
Variablefissure* 89.1% 0.65 0.53 ; 0.76 < 0.001 95.4% 0.84 0.72 ; 0.95 < 0.001
flaking 79.7% 0.54 0.37 ; 0.71 < 0.001 91.8% 0.83 0.67 ; 0.98 < 0.001
posterior fold disruption 83.2% 0.51 0.32 ; 0.70 < 0.001 92.1% 0.74 0.57 ; 0.90 < 0.001
haemarthrosis 87.3% 0.48 0.32 ; 0.64 < 0.001 98.7% 0.88 0.72 ; 1.04 < 0.001
bleeding in folds 81.6% 0.36 0.23 ; 0.49 < 0.001 97.3% 0.84 0.72 ; 0.96 < 0.001
split 72.9% 0.31 0.15 ; 0.47 < 0.001 89.9% 0.79 0.63 ; 0.94 < 0.001
vascular invasion 82.1% 0.29 0.13 ; 0.45 < 0.001 93.0% 0.70 0.55 ; 0.86 < 0.001
facet fracture 87.4% 0.23 0.12 ; 0.34 < 0.001 99.4% 0.85 0.70 ; 1.01 < 0.001
blood in subchondral bone 81.3% 0.15 0.00 ; 0.30 < 0.05 88.4% 0.59 0.44 ; 0.74 < 0.001
osteochondral fissure 56.0% 0.13 -0.01 ; 0.27 < 0.05 82.8% 0.61 0.46 ; 0.75 < 0.001
anterior fold disruption 84.6% 0.09 -0.08 ; 0.26 0.156 94.9% 0.75 0.59 ; 0.91 < 0.001
osteophytes 91.9% -0.04 -0.21 ; 0.13 0.688 96.8% 0.65 0.50 ; 0.80 < 0.001
*: weighted kappa
95% CI 95% CI
Interobserver agreement Intraobserver agreement
Table 7.5 Inter- and intraobserver agreement regarding microscopy of morphological variables
70
8. Discussion
8.1. Diagnostic imaging of the cervical spine facet joints after trauma
Using conventional X-rays, CT and MRI this study identified several lesions in the lower cervical spine
facet joints of road traffic crash fatalities in comparison to non-traumatised decedents, thereby
supplementing the results from previous advanced imaging studies 30;46;168;169;178;231. Fractures of the
articular facets were identified in four subjects (4/19 trauma cases) using diagnostic imaging techniques
which is a somewhat higher prevalence rate than reported in previous studies 30-32;36;46;169;178;231. As only
one of the facet fractures were identified on conventional X-rays the inadequacy of this imaging modality
towards visualising this type of lesion was underlined which is in agreement with previous findings
26;40;164-166;186;192-198. This finding strongly suggests that previous studies based solely on conventional X-
ray examination may have been significantly influenced by under-reporting of facet fractures. However,
although CT was the most sensitive imaging modality towards identifying facet fractures, similar to other
studies 164-168, only four of the 11 unique facet fractures identified on microscopy could be visualized
suggesting that, when present, facet fractures are more often affecting several facets rather than solitary
levels and that CT may miss discrete fractures 168;184. Hence, the overall sensitivity of advanced
diagnostic imaging procedures is inferior to microscopical examination with regard to the identification of
discrete facet fractures in the lower cervical spine.
This study revealed that post-mortem diagnostic imaging procedures, including MRI, do not reliably
identify injuries to the synovial folds or cases with haemarthrosis in comparison to the microscopical
findings, which has been reported previously 30-32;36;46;112;115;178;231. This was despite optimal imaging
conditions with no motion artefacts, long acquisition times and several different protocols including
sensitive STIR sequences. In contrast, a recent study identified the cervical spine facet joint folds on
MRI, although this required a high energy-field 3.0 Tesla MRI unit, with long acquisition time, limited field
of view and a small specimen size 117. In the current study a 1.5 Tesla MRI unit was used and the
protocols used may not have allowed adequate resolution introducing technical limitations that may have
71
affected the observations 117;168. Possibly, these findings suggest that increased signals in the facet joints
spaces in post-mortem subjects are unspecific, potentially irrelevant findings in relation to pre-mortem
status of these joints. However, as a large number of the trauma cases (almost half) had incurred
haemarthrosis and/or bleeding in the synovial folds (evident on microscopy) lesions were present in
many cases although they could not be verified reliably. In contrast to these findings, previous studies
have identified bleeding in the cervical spine facet joints on MRI in people killed in road traffic crashes,
using both independent observations and blinding to the pathological findings although the findings were
not statistically tested 178. In none of the conventional X-ray or CT investigations did the observers
identify soft tissue injuries in the facet joints.
The agreement between the observers with regard to detection of facet fractures was good for all
imaging modalities. The substantial agreements between the initial findings (the first evaluation) and the
consensus findings (the second evaluation) obtained by each observer supports the opinion that the
radiological findings of facet fractures are credible. In contrast, the observers obtained a poor agreement
with regard to the presence of bleeding/excess fluid in the joint on MRI. As this was thought to be a
problem of definition the observers agreed upon improved criteria prior to the third evaluation of
bleeding/excess fluid in the joint on MRI only. However, this did not improve the interobserver agreement
and comparing the results between the two evaluations poor intraobserver agreement was obtained,
which was probably explained by the newly introduced criteria. Actually, using the consensus criteria with
regard to scoring the MRI images for haemarthrosis/excess fluid in a joint, a significant increase in the
number of joints positive for this variable was observed with no correlation to trauma, suggesting either
improper definition of the variable or clinically irrelevant structural changes at post-mortem. Furthermore,
the integrity of the synovial folds could not be evaluated as these were not visualised specifically on any
of the imaging modalities. Overall, MRI of the soft tissues of the facet joints did not offer reliable
information and the role of this modality in the post-mortem evaluation of facet joint soft tissue injury is
questionable. This finding must be regarded in the context of the high frequency of soft tissue lesions in
the traumatised subjects (approximately half had soft tissue injuries). However, the role of MRI in the
evaluation of soft tissue injuries to the facet joints may have different relevance in clinical settings.
Survivors of road traffic crashes may sustain injury to the soft tissues of the facet joints that is likely to
cause hyperaemia, oedema, swelling, inflammation and pain developing over hours to days.
Theoretically, this should improve the likelihood of diagnosing injury to these joints as these processes
72
introduce physiological and potentially structural changes. Nonetheless, the findings from this study
suggest that soft tissue lesions in the facet joints, including haemarthrosis and bleeding in the synovial
folds, are difficult to diagnose on MRI.
No previous studies have published inter- and intraobserver agreement scores of the radiological
examination of post-mortem cervical spines nor the exact effect of training of observers with regard to
scoring of forensic radiological images, although recent comments in this regard have been proposed 168.
However, a recent clinical study evaluated the reliability of in vivo CT-scanning, in which a clinical
classification system for lower cervical spine injuries based on conventional radiology and CT-scanning
was proposed based on excellent intra- and interobserver agreement 232. Hence, although a comparison
with the findings from the current study is impossible future trials should evaluate the reliability of post-
mortem diagnostic imaging findings in order to ensure quality control.
The current generation of multislice CT-scanners (i.e. 64 slice scanners) typically produce image slice
thicknesses of 0.64 mm, which is a considerable improvement in comparison to the four-slice scanner
used in this study, and with the enhanced resolution the diagnostic sensitivity can be expected to
increase significantly. However, despite these advancements in CT technique, the specificity and
sensitivity of negative clinical and post-mortem CT examinations remains questionable as particularly
discrete injuries in the soft tissues of the facet joints were very common in the trauma cases without
being identified on the CT.
8.2. Pathology of the cervical spine facet joints after trauma
This study identified a total of 11 unique facet fractures in four of 19 subjects exposed to a fatal road
traffic crash, which is somewhat higher than previously reported 30-32;36;46;169;178;231. For example, in one
study examining road traffic crash fatalities, one lower cervical spine facet fracture was detected in one
of 22 crash victims 32. In another study, four unique lower cervical spine fractures were identified in one
subject out of 15 examined 36. The differences between the reported figures are likely due to sample
size, population characteristic (e.g. age and gender) anatomical region of interest and the mechanisms of
trauma, where the exposure to a road traffic crash causing life-threatening injuries and death indicates
the exchange of forces of a substantial magnitude. Hence, in this study all the trauma subjects were
young and had been occupants of a passenger car, which had crashed subjecting the decedent to fatal
bodily injuries.
73
The presence of haemarthrosis of the cervical spine facet joints have previously been described in post-
mortem studies of road traffic crash victims using histological and/or microtomal methods 30-32;36;46;178;231,
although the incidence rates have not previously been estimated. However, as haemarthrosis has not
generally been confirmed by histological evaluation in studies using cryomicrotomy these findings may
not be comparable. In this study, haemarthrosis was confirmed by the presence of erythrocytes in the
joint cavity which in some cases was difficult. Therefore, comparison with blood vessel content allowed
identification of erythrocytes as pale cell ghosts in a honeycomb pattern and by this definition
haemarthrosis was identified in almost half the trauma cases with statistical significance. This may
however have caused underestimation as tissue necrosis may have caused the erythrocytes to be
interpreted as decomposed synoviocytes and debris in the joint rather than blood. Nonetheless, the high
incidence of haemarthrosis in the trauma group was statistically significant in this study indicating that
these findings are common following fatal road traffic crashes with or without the presence of facet
fracture. The presence of bleeding in a joint has been shown to have negative effects on the cartilage, as
even brief exposures to blood may have detrimental long-lasting effects on the cartilage, by inhibiting the
proteoglycan synthesis, thereby predisposing to premature degeneration 233-236. Hence, acute synovitis
after haemarthrosis and/or cartilage damage may occur after trauma 233;236, which may also have
relevance for development of neck pain following adequate trauma.
The finding of bleeding in several folds is similar to previous reports 27;30-32;36;46;178. However, in some of
the control subjects bleeding was also encountered indicating that artefacts are being produced during
handling of the decedent or that this may be a natural physiological post-mortem finding. Despite this
finding, bleeding and disruption of the synovial folds correlated significantly to the exposure trauma. This
suggests that the folds are at risk of injury during a fatal road traffic crash. Although this may seem
irrelevant in a forensic perspective, this may have clinical implications as the folds are nociceptive
structures which may explain neck pain at least in the acute phase in casualties after survivable road
traffic crashes 36;37;107;113;114;119.
The presence of horizontal split of the articular cartilage was also closely related to trauma. As the
cartilage does not receive sensory nerve supply these lesions do not directly cause pain. However, it can
be conjectured that such lesions predispose to degeneration of the articular facets as the internal
architecture is disorganised with consequently altered biomechanics of the cartilage 122;124.
74
Theoretically, the advanced degenerative changes observed on diagnostic imaging of chronic neck pain
patients following survivable road traffic crashes 211-213, may be explained by the potential consequences
of any of the findings including; cartilage split, facet fractures, haemarthrosis as well as disruption of
synovial folds. These conditions may alter the biomechanics of the articular cartilage and the joint
whereby degradation of cartilage matrix may predispose to OA years after the injury 33;114;212;213;237.
Stereomicroscopic evaluation of plastic embedded 3-mm thick slices were found unreliable with regard to
the identification of osseous and/or soft tissue injury to the lower cervical spine facet joints, and findings
from previous reports could not be confirmed. Hence, light microscopy was found superior to
stereomicroscopy in the evaluation of pathology of the lower cervical spine facet joints.
The conventional medicolegal autopsy, which utilised an anterior approach 225, did not identify any of the
injuries in the cervical spine facet joints despite histological and neuroradiological evidence of injuries.
However, the poor sensitivity towards identifying injuries in the facet joints is not surprising as
conventional medicolegal autopsy does not allow detailed description of the posterior elements of the
cervical spine. This is in accordance with other studies reaching the same conclusions regarding
standardised autopsies 30;31;36;46;178;238. Hence, post-mortem investigations of cervical spine injury
necessitate detailed autopsy procedures similar to those utilised in this study.
8.3. Anatomy of the lower cervical spine facet joints
In this study, morphological and histomorphometric evaluation of the lower cervical spine facet joints
revealed a number of age and gender related differences in anatomical properties.
The mean articular cartilage thickness of the cervical spine facet joint at C4 inferior process was
approximately 0.8 mm, independent of gender, but depending on the spinal level. In a related study the
mean overall thickness of the cervical spine facet cartilage was found to be less (females 0.4 mm and
males 0.5 mm) 48. However, these findings were based on a cryomicrotomal study of six elderly
embalmed cadavers which makes precise determination of the cartilage thickness difficult as the
measurements are performed on photographic illustrations. The differences observed in the current
study between the spinal segments probably are consequences of developmental adaptations to
different functional requirements depending on the spinal segment. It was interesting to observe that the
calcified cartilage occupied approximately 10 % of the complete cartilage thickness which is somewhat
higher than previous studies of other joints reporting values of approximately 5 % (3-8 %) 127-129. The
75
finding of anterior and posterior synovial folds in all but one joint, irrespective of age and gender,
supports a number of previous publications 47;107;116;117;135. In contrast to these findings other studies have
not been able to identify synovial folds consistently in the facet joints 112;185. Fletcher et al 185, examined
20 cadavers (two aged 10 and 19 years, and the remaining 18 subjects between the age of 37-86 years)
with photographic documentation of cryomicrotomal sections and haematoxylin-eosin staining of
decalcified sections and concluded that the menisci [folds] were nonexistent at the age of 37 years and
older. In the study by Yu et al 112, 10 decedents (mean age 48 years, range 10-69 years) were examined
with photographic evaluation of cryomicrotomal sections and four types of menisci [folds] were proposed
despite the low number of subjects and the authors concluded that in the lower cervical spine of adults,
no menisci [folds] were present within the joint and the articular surfaces. Hence, both these studies
relied on photographic documentation, which probably in part explains their results. Similarly, all the folds
had a mean overlap of approximately 16 % of the underlying cartilage. However, in several parasaggital
sections of the facets the synovial fold covered the articular surface completely which indicates that the
folds have a heterogenous covering of the articular surface. The consistent presence of the synovial
folds suggest that they may have a unique physiological function, similar to the protective and lubricative
function of menisci, although this has not been elucidated 33;107;239.
Hyaline cartilage was found to cover the joint surfaces in the majority of the joints. Occasionally, a
transitional zone was observed at the borders of the cartilage covering of the facets in which a gradual
replacement of the hyaline cartilage by fibrous cartilage took place. Hence, only rarely were free bony
edges encountered with periosteal covering, previously described as “cartilage gaps” 48. The
discrepancies between these findings may be explained by the different populations examined, where
the previous study only included six elderly subjects in contrast to this study’s 40 subjects in the age
range 20-49 years, and the orientation of sectioning (although both methods used parasaggital
orientation). It is believed, that detailed morphology is best visualised by microscopy rather than by
evaluation of photographic reprints of anatomical structures. It can be speculated that the previously
reported findings are due to technical limitations, i.e. poor resolution, which does not allow identification
of all articular cartilage and fibrous cartilage. Hence, the current study does not offer support for the
presence of cartilage gaps and consequently no support of the pathomechanical theory of bony impact
during trauma as a cause of persistent neck pain.
76
A number of morphological variables were significantly correlated with age, including; cartilage flaking,
cartilage split, and osteophytes, and are all related to OA 49;122;131. The commonest finding was flaking of
the cartilage, followed by cartilage split and fissures, all present in more than half the articular facets,
indicating that these changes occur early in life. Age was also significantly related to an increase in the
subchondral bone thickness, although no age-related differences were observed concerning the
thickness of the hyaline and calcified cartilage. The subchondral bone thickness increased approximately
10 % per decade which is in agreement with previous observations 122;127;129. Other indicators of OA,
such as osteophytes, duplication of the tidemark and vascular invasion of the tidemark, were only
present in limited numbers which is explained by the median age (35 years) of the entire study
population. However, despite the young population examined, cartilage flaking, split and fissures were
very common in all ages in agreement with other studies 49;130. Although, fissures were common they did
not reach significant correlation with age despite published correlations with OA and increasing age
122;131.
The overall finding of significant correlation between gender and histological findings seen in OA (e.g.
cartilage flaking and splitting) is in agreement with other reports of males having a preponderance for
pathological facet joints, i.e. males were more severely affected by these changes than females 49;122.
Similarly, the cartilage length was significantly shorter in females which has also been reported
previously 54;56. Nonetheless, several variables were not affected by gender; e.g. overlap of the synovial
folds, and the thickness of the articular cartilage and the subchondral bone.
8.4. Methodological considerations
The effective study population consisted of 40 subjects, providing a total of 636 unique lower cervical
spine articular facets, which considering the fact these were post-mortem human subjects is a quite high
number. In order to improve the likelihood of obtaining significance of the statistical analyses we used
strict inclusion criteria, which produced a homogenous group of subjects. Although this increased the
statistical strength this also had a detrimental effect as a number of biological age-related variables (e.g.
osteophytes) were much less likely to be observed in this population of a median age of 35 years (range
20-49). Furthermore, the population size did not allow evaluation of the potential effects of interaction in
relation to age, as the statistical significance was not present. The difference from time of death to time
of autopsy, the influence of outside temperature and surroundings was not taken into consideration in
77
this study. Although advanced decomposition was an exclusion criterion, two subjects had to be
excluded after inclusion due to advanced tissue decomposition, which was identified on microscopical
examination and combined with the findings during autopsy. It can be difficult to evaluate the exact
extent of putrefaction in a body, since the early changes in particular may vary according to anatomical
region. Nonetheless, it is a prerequisite for comparability that the subjects are in a comparable state
exhibiting only limited post-mortem changes.
In this study the most common cause of death in the trauma group was multiple injuries with a high
incidence rate of skull fractures and organic injuries. Forensic toxicology revealed that four of the 18
drivers killed were under the influence of alcohol during the time of the crash which is similar to
previously reported figures of 20-30 % of decedents from fatal road traffic crashes having BAC values
above 0.5 mg/ml 240-242. Similarly, we found one trauma case who tested positive for drugs which also
supports previous reports of drugs in road traffic crash fatalities 241. Hence, the subjects included in this
study were comparable with road traffic crash fatalities examined in other studies 60;138.
This study was performed on tissue samples that had been removed en bloc from the decedent, rather
than examined in situ. Removal of tissue samples from decedents is known to enhance the rate of
putrefaction in the tissues. Although this may have influenced the quality of the diagnostic images and
the following histological samples the detrimental effect hereof is thought to be minimal since the
samples were examined within 24 hours, most often within two to four hours after removal. Furthermore,
cooling of the samples was used until diagnostic imaging after which fixation was initiated immediately.
When preparing bone samples for microscopical examination of un-decalcified stained sections, paraffin
embedding cannot be utilised since this does not supply adequate support of the osseous tissue during
microtomy. Therefore, alcohol (ethanol) fixation followed by embedding in liquid methylmethacrylate was
chosen as the most suitable method. Nonetheless, we found that fixation was extremely time-consuming
and that the quality of the consequent histological sections probably was affected by the quality of
fixation of these large specimens.
Embedding large tissue samples in MMA demands skill and experience as the process takes place over
several weeks. In some cases the polymerisation (hardening) of the MMA had not been completed
evenly throughout the bloc, which made consequent sawing difficult with the risk of inducing artefact in
the tissues. Alternative methods have been used extensively in the last couple of decades which involves
cryosectioning (cryomicrotomy) of frozen samples rather than fixation 28;32;48;184;185;243-245. However, for the
78
purpose of the present study this method would require a large cryomicrotome, which was only present
in Denmark in one centre (privately owned) at the start of the project. It is however interesting whether
future studies would be able to utilize such apparatus, as that would significantly reduce the time factor.
Furthermore, cryosectioning may perform automated continued sectioning throughout a specimen of a
set thickness, e.g. 50 μm, with the production of a few microns thick section per interval, which may be
stained prior to microscopy.
We found that staining the plastic mounted histological sections with Masson-Goldner trichrome or
haematoxylin-eosin did not visualise the erythrocytes, as they would normally appear on a conventional
section, e.g. paraffin embedded pulmonary tissue sample. It was speculated that the remaining plastic in
the histological sections caused incomplete staining of the erythrocytes, however staining of sections
without plastic did not influence the staining characteristics. Possibly, the prolonged ethanol fixation and
embedding period may have resulted in osmotic gradients and dissolution of the erythrocyte cells
whereby consequent staining of un-deplastified histological sections may have caused the poor
visualisation of erythrocytes in the lesions sites thereby underestimating bleeding.
From other histological studies it is known that tissue may shrink during handling 246. As shrinkage most
often takes place non-homogenously within tissue samples this is likely to have affected the results in
this study. However, no attempts to quantify the effects of shrinkage were made.
We evaluated the histomorphometrical properties of the articular cartilage, the calcified cartilage and the
underlying subchondral bone in typically 9-12 locations of each cervical spine facet between C4 and Th1.
However, although the histological sections were produces from random lines through the facets the
orientation was not completely randomised, i.a. all lines were parasaggital and parallel. Other studies
have used the same direction of sectioning (i.e. parasaggital) 27;31;32;48;135;178;185, and only few studies
have used supplemental planes of sectioning 36. Although we randomised the locations of measurements
the effect of orientation is unclear. Consequently, systematic false readings could be obtained due to the
line of sectioning chosen as this may skew the true anatomical sizes and appearances. Preferably, a
stereological unbiased evaluation using random sampling and orientation should be used in order to
examine a larger population with a wider age-range for the extent of age-related changes.
Notwithstanding these facts, we believe that our results are acceptable estimates of the
histomorphometry of the lower cervical spine facet joints, and they provide a systematic presentation of
the cartilage, subchondral bone and soft tissue properties.
79
The potential consequences of a three-dimensional structure (i.e. the facet joint) being sectioned in one
plane for the purpose of two-dimensional evaluation likewise affect the morphological interpretation.
The morphological variables were evaluated dichotomously, with the exception of few variables where
more possibilities were present. For example, it is conceivable that the synovial folds identified in the
anterior and posterior parts of the joints are continuous circular structures surrounding the entire surface
of the cartilage, rather than only located anteriorly and posteriorly. This would not be detectable using the
current methods. Furthermore, as a consequence of the thickness of sawing (i.e. 3-mm thick slices) facet
fractures parallel to the line of sectioning would not necessarily appear on the histological sections as
discrete fractures could be present inside the 3-mm slices but outside the area of consequent microtomal
sectioning.
The purpose of this study was not to design a scoring system for the histological grading of OA in the
facet joints. However, using a pragmatic approach several morphological variables known to have
relevance to OA were selected and described. The method used in this study did not allow evaluation of
the true severity of the morphological variables as only the worst case finding was recorded for each
observation. A recently proposed classification system, by the OARSI Working Group, integrates the
grade (extent) and stage of degenerative changes in general cartilage with limited considerations to the
subchondral bone 131. Grading and staging of age-related and OA changes in the cervical spine facet
joints may be performed with the method of Pritzker et al 131. However, this system is based upon
examination of decalcified paraffin embedded sections rather than un-decalcified plastic embedded
sections which makes the method inappropriate for the evaluation of large un-decalcified osteo-
cartilaginous specimens. Ideally, however, severity measures should be integrated in the method by
considering the extent of tissue affected 131. Hence, an adjusted classification system based on the
principles of the OARSI Working Group methods targeting the cervical spine facet joints specifically
seems to be the most ideal solution 131.
An alternative scoring system for cervical spine facet joint OA has been published 135. However, the
weighted contributions from each variable were accumulated whereby the likelihood of observing
differences in pathological severity between individuals was reduced. This probably explains why
insignificant differences were identified between age groups and severity of the changes.
In the evaluation of inter-observer agreement between a senior pathologist and the lead investigator
generally moderate agreement was achieved for the majority of the morphological variables. The
80
interobserver agreement was probably influenced by improperly defined variables as well as different
levels of experience between the observers in combination with the low prevalence rate. For example,
the osteophytes identified were discrete changes rather than the typical appearance of large bony spurs,
hence differentiation of positive versus negative scoring was difficult, even within the same observer.
Similarly, osteochondral fissures were believed to have little, if any, biological relevance as they most
often were unstained empty spaces indicating artefacts rather expression of true anatomical morphology.
Hence, the observers may have scored the osteochondral fissures differently, depending on whether
they were regarded as true fissures rather than artefacts. Excessive bleeding in the subchondral bone
was extremely difficult to confirm, as the presence of blood was a frequent normal finding. We can offer
no sensible explanation why the integrity of the anterior folds could not be established reliably between
the observers as the evaluation of the posterior counterpart resulted in a higher and significant
agreement score. The overall intraobserver agreement was good, and for all variables better than the
interobserver agreement, which could be expected. Despite the overall acceptable inter- and
intraobserver agreement scores, future studies should attempt to improve the definitions of the variables
in consensus. Furthermore, the analysis underlines the importance of training and consensus of
definitions of the anatomical structures under investigation.
Initially attempts were made to compare the results from the investigation of the cervical spine facet
joints and pathological evaluations with data from the police records with regard to the mechanism of
trauma. However, in far the majority of the road traffic crash cases the mechanisms of trauma were
complex and the extent of bodily injury was significant. Furthermore, only limited information concerning
the details of the fatal crashes were available which did not allow optimal correlation of the findings from
our study to the police records. Hence, future studies investigating the specific causative mechanisms of
trauma in relation to unique pathological findings need to address these difficulties early in the planning
phase, as detailed onsite investigations of the crash is necessary for adequate information pertaining to
the crash scene and circumstances.
8.5. External validity and clinical implications
It is clear from this study that the cervical spine facet joints have a unique morphology which is probably
closely related to the highly specialised physiological (biomechanical) demands. With consideration to
the methodological limitations in this study, the findings are thought to be in good agreement with
81
previously published studies and therefore reliable measures of the anatomical properties of the facet
joints.
Regarding the pathological findings uncritical extrapolation from post-mortem findings to survivors
sustaining similar injuries cannot be justified. However, it is interesting to consider whether the
pathological findings in this study are likely to be present in survivors of RTC’s, and whether such
discrete injuries have clinical implications.
A number of studies have found similar lesions in survivors from road traffic crashes who later died due
to un-related causes 26-29;139;169, and clinical studies using diagnostic imaging procedures have identified
osseous injuries in survivors from road traffic crashes 41. Biomechanical studies have pointed to
pathological force loading on facet joint structures as a consequence of the exposure to relatively minor
acceleration forces 69-71;78;79. Furthermore, in clinical practice, posterior neck pain is an extremely
common symptom following RTC’s for which specific organic causes seldom can be documented
21;25;156;157. Hence, these findings converge on the theory that injuries are likely to be incurred based on
violent acceleration-deceleration forces to the cervical spine complex and that these injuries may well
arise in traumas that expose the occupants to forces short of lethal forces 21;30;95. However, the frequency
of facet joint fractures and soft tissue lesions in humans subjected to cervical spine acceleration-
deceleration forces in survivable RTC’s is unknown 21;30;34.
Although this study has not studied the classical whiplash trauma (LOSRIC) per se, it has investigated
injuries that may be related to motor vehicle crashes of a wide range of severities. It is noteworthy that
not all decedents due to a road traffic crash suffered significant external evidence of neck, head and/or
brain injury. As a matter of fact, in several cases the primary cause of death was not related to lesions in
the head or neck. Hence, it is conceivable that the discrete non-fatal injuries of the lower cervical spine
facet joints detected in this study of high-energy crash fatalities would also have been present had the
decedents been exposed to sub-lethal forces to other vital organs in which the primary cause of death
was identified.
Causal injury thresholds for facet fractures and soft tissue injuries of the lower cervical spine facet joints
are not available as these are dependent upon many factors 14;95;96;247. The majority of whiplash trauma’s
involve the exchange of relatively low energy (force) 14;59;63-65, and presumably the average resultant
forces acting on the occupants subjected to a LOSRIC are much less than what is expected to have
been inflicted on the fatalities in this study. This is probably also the case for the loading of the facet
82
joints in the lower cervical spine. However, as the forces in common rear-impact collisions involve
pathophysiological compressive, distractive and shear forces to the facet joints 37;77-80;82 the differences
in magnitude of loading between the different types of crashes cannot be evaluated based on this study.
Hence, as the individual thresholds of injury for any particular subject under any given crash
circumstances cannot be reliably estimated 95, the findings in this study may well have relevance and
clinical implications for subgroups of people injured in whiplash trauma.
83
9. Conclusions and perspectives
This study provided a detailed description of the histomorphology of the lower cervical spine facet joints
of a young population with regard to the soft tissues, cartilage and subchondral bone. Degenerative
changes in the facet joints were found to occur early in life in both the cartilage and the subchondral
bone. Two synovial folds were identified in all but one facet joints which indicate a yet unproven
biological function. The calcified cartilage was constantly equal to about 10 % of the total articular
cartilage thickness and the articular facets were generally covered in their entirety by primarily hyaline
cartilage.
The original hypothesis that there is an under-representation of pathoanatomical lesions in the cervical
spine facet joints in people killed in road traffic crashes examined by standardised autopsy and
conventional radiological evaluation was confirmed. Non-fatal injuries to the lower cervical spine facet
joints were common in road traffic crash fatalities, including facet fractures, haemarthrosis, disruption and
bleeding in the synovial folds. The lesions were best appreciated on light microscopy in comparison to
stereomicroscopic evaluation, and conventional autopsy procedures did not reveal any of the injuries.
Discrete osseous lesions in the lower cervical spine facet joints were detected in people killed in
passenger car crashes by means of advanced diagnostic imaging procedures, including conventional X-
rays, magnetic resonance imaging, and in particular computed tomography. However, approximately half
of the unique facet fractures were not detected on any imaging modality despite optimal technical
circumstances, confirming that not all discrete facet fractures are identified on diagnostic imaging
procedures. Furthermore, bleeding in the cervical facet joints and synovial folds could not be determined
reliably on any diagnostic imaging modality, including MRI, despite histological evidence hereof. This
study emphasizes the need for scientific evidence of validity and reliability of advanced diagnostic
imaging procedures in forensic settings, in particular with regard to non-fatal soft tissue lesions.
The data concerning the circumstances of the traffic crashes were insufficient in order to conduct
detailed comparison with the pathological findings, as the majority of decedents killed in a road traffic
crash suffered multiple injuries due to complex kinematics and force loading.
84
The utilisation of increasingly advanced imaging modalities as well as specialised autopsy techniques
should be encouraged in forensic settings in order to increase the sensitivity towards identifying discrete
injuries. The potential clinical implications of the lesions identified in this study are unknown. However,
although uncritical extrapolation of the results to survivors from road traffic crashes cannot be justified, it
is plausible that discrete injuries similar to those identified in this study will be present in subgroups of
casualties from survivable road traffic crashes.
85
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243. Jonsson H, Jr., Rauschning W. Postoperative cervical spine specimens studied with the
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105
Appendix 1
Facet fractures on radiology and histology
RADIOLOGY (CONSENSUS) HISTOLOGY
Subject Age Gender Facet facture
on X-ray Facet facture
on CT Facet facture
on MRI Facet fracture on
10 μm 26 21 M No No No No 24 22 F No Yes Yes No 35 33 M No No No No 14 20 M No No No No 20 29 M No No No No 25 36 M Yes Yes Yes Yes 42 29 M No No No No 47 23 F No No No No 21 31 F No No No No 13 34 M No No No No 17 45 F No No No No 19 35 M No No No No 22 20 M No No No Yes 36 29 M No No No No 46 37 M No No No No 53 31 M No Yes Yes Yes 39 41 M No Yes No Yes 34 47 M No No No No 28 38 M No No No No 19 cases 1 4 3 4 16 39 F No No No No 48 46 F No No No No 12 41 M No No No No 29 34 F No No No No 43 33 M No No No No 30 43 F No No No No 38 49 M No No No No 18 37 M No No No No 45 35 M No No No No 51 23 M No No No No 15 32 M No No No No 23 37 M No No No No 31 31 M No No No No 44 40 M No No No No 52 48 M No No No No 50 41 F No No No No 49 41 F No No No No 40 27 F No No No No 54 22 M No No No No 37 49 F No No No No 33 35 M No No No No 21 controls 0 0 0 0
Gender: male (M), female (F)
App
endi
x 2
Info
rmat
ion
from
the
polic
e re
cord
s co
ncer
ning
the
road
traf
fic c
rash
fata
litie
s
106
Subj
ect
Mon
thAc
tion
# in
volv
ed
part
ies
# ki
lled
# ca
sual
ties
Roa
d co
nditi
ons
Visi
bilit
yLi
ght
Wea
ther
Allo
wed
sp
eed
km/h
Shap
e ro
adC
ircum
stan
ces
Type
of r
oad
Prim
ary
colli
sion
po
int
Estim
ated
spe
ed
km/h
26no
vem
ber
pass
enge
r2
13
dry
good
dark
ness
no ra
in70
stra
ight
obst
acle
mai
n ro
adrig
htun
know
n
24no
vem
ber
driv
er2
17
wet
good
dayl
ight
no ra
in80
stra
ight
front
al k
ollis
ion
mai
n ro
adfro
ntun
know
n
35ja
nuar
ydr
iver
11
0w
etgo
odda
ylig
htno
rain
110
stra
ight
obst
acle
mai
n ro
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ntun
know
n
14ja
nuar
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iver
11
0ic
ygo
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ssno
rain
80st
raig
htso
lom
ain
road
com
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dun
know
n
20ja
nuar
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iver
21
4dr
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ygo
odda
rkne
ssno
rain
50st
raig
htfro
ntal
kol
lisio
nci
ty ro
adfro
nt40
25m
aydr
iver
21
0dr
ygo
oddu
skno
rain
80st
raig
htfro
ntal
kol
lisio
nm
ain
road
front
80
42se
ptem
ber
driv
er2
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dry
unkn
own
dusk
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own
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raig
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ntal
kol
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nm
ain
road
front
unkn
own
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cem
ber
driv
er1
11
wet
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dark
ness
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in80
stra
ight
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acle
mai
n ro
adco
mbi
ned
unkn
own
21ja
nuar
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iver
21
0ic
yre
duce
ddu
skno
rain
80cu
rve
front
al k
ollis
ion
mai
n ro
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mbi
ned
70
13ja
nuar
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iver
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nm
ain
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own
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iver
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rain
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untry
road
front
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own
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arch
driv
er2
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wet
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ness
rain
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nm
ain
road
front
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own
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rildr
iver
11
0dr
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rkne
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rain
80st
raig
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lom
ain
road
com
bine
dun
know
n
36m
aydr
iver
21
1dr
ygo
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ylig
htno
rain
80st
raig
htfro
ntal
kol
lisio
nm
ain
road
front
unkn
own
46no
vem
ber
driv
er2
12
wet
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dark
ness
no ra
in80
inte
rsec
tion
side
impa
ctm
ain
road
left
unkn
own
53de
cem
ber
driv
er1
10
wet
good
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ness
no ra
in80
curv
eob
stac
lem
ain
road
left
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own
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arch
driv
er1
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dry
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ness
no ra
in80
curv
eob
stac
lem
ain
road
com
bine
dun
know
n
34ap
rildr
iver
11
0dr
ygo
odda
ylig
htno
rain
80cu
rve
solo
mai
n ro
adco
mbi
ned
unkn
own
28m
aydr
iver
31
2dr
ygo
oddu
skno
rain
130
stra
ight
com
bine
dhi
ghw
ayco
mbi
ned
unkn
own
Appendix 3
Toxicological findings
Trauma cases
Subject Age Gender Blood alcohol
concentration (‰) Drugs/ medicine
in blood and/or urine
26 21 M 2,08 No
24 22 F 0,00 No
35 33 M 0 No
14 20 M 0,88 No
20 29 M 0,10 Not tested
25 36 M 0,90 Metoprolol
42 29 M 0 Not tested
47 23 F 0 Not tested
21 31 F 0 No
13 34 M 0 Ketamine¥
17 45 F 0 Not tested
19 35 M 1,89 Not tested
22 20 M 0 Valproate
36 29 M 0 Not tested
46 37 M 0 Not tested
53 31 M 0,22 Not tested
39 41 M (2,40)± Not tested
34 47 M 0 Citalopram
28 38 M 0 Not tested 19 cases 5 (BAC>0.5) 4
Controls
16 39 F 0 Not tested
48 46 F 1,82 No
12 41 M 0,78 Not tested
29 34 F 1,80 Cannabis¥
43 33 M 0 Not tested
30 43 F 0 Clomipramine & paracetamol†
38 49 M 0 Not tested
18 37 M 0 No
45 35 M 0 No
51 23 M 0 Not tested
15 32 M 0 No
23 37 M 0 Not tested
31 31 M 0 Not tested
44 40 M 0,28 Not tested
52 48 M 0 Not tested
50 41 F 0 Not tested
49 41 F 0 No
40 27 F 0 Cocaine¥
54 22 M 0 No
37 49 F Not tested Not tested
33 35 M 0 No 21 controls 3 (BAC>0.5) 3
BAC: Blood alcohol concentration Gender: M (male), F (female) ± conc. in eyefluid (vitrous humor) † conc. of intoxication (overdose) ¥ narcotics/drugs
107
Imaging occult lesions in the cervical spine facet joints
Lars Uhrenholt, DC1,2,3, Edith Nielsen, MD4, Annie Vesterby Charles, Professor, DMSc.1,3,
Ellen Hauge, PhD, MD3,5,, Markil Gregersen, Professor, DMSc.1
1 Institute of Forensic Medicine, University of Aarhus, Denmark
2 Nordic Institute of Chiropractic and Clinical Biomechanics, Part of Clinical Locomotion Science, Odense,
Denmark
3 Research Unit of Rheumatology and Bone Biology, Aarhus University Hospital, Aarhus Sygehus (NBG),
Denmark
4 Department of Neuroradiology, Aarhus University Hospital, Aarhus Sygehus (NBG), Denmark
5 Department of Rheumatology, Aarhus University Hospital, Aarhus Sygehus (NBG), Denmark
Corresponding author:
Lars Uhrenholt
Institute of Forensic Medicine
University of Aarhus
Brendstrupgaardsvej 100, 8200 Aarhus N, Denmark
E-mail: lu@forensic.au.dk
Facsimile: 45-86125995, Phone: 45-89429800
PAPER I
page 2
Abstract
Discrete injuries in the lower cervical spine facet joints have been reported in studies of motor vehicle crash
victims. We conducted a detailed investigation of these joints from 20 motor vehicle crash fatalities and 22
decedents due to non-traumatic causes using conventional radiology, computed tomography and magnetic
resonance imaging in order to examine whether the diagnostic imaging procedures could identify injuries in
the facet joints. The diagnostic imaging procedures identified facet joint fractures in 4 of the 19 trauma cases
with computed tomography having the highest sensitivity and obtaining good correlation with findings from
the microscopical evaluation. No diagnostic imaging procedure could reliably evaluate the integrity of the
synovial folds or the joint spaces for bleeding despite microscopical evidence of such findings in these
structures in a large proportion of the motor vehicle crash fatalities. This study emphasizes the need for
scientific evidence of validity and reliability of advanced diagnostic imaging procedures in forensic settings, in
particular with regard to occult soft tissue lesions, and cautions uncritical use of negative results from these
procedures until such evidence has been produced.
page 3
Introduction
One of the primary functions of radiological evaluation in forensic medical settings is to confirm the presence
or absence of fractures in victims from assaults, and investigate road traffic crashes, child abuse cases and
other criminal or suspect cases1. With Computed Tomography (CT) and Magnetic Resonance Imaging (MRI)
procedures more detailed analysis can be performed, compared to previous methods such a conventional x-
rays, and these procedures are being utilised increasingly in forensic settings around the world2-5.
Furthermore, diagnostic imaging findings, such as typical skull fractures, spinal and extremity fractures can
often be verified by localised incision of the lesion site2;4. However, recent studies have suggested that
discrete injuries in the spinal column may remain undetected on advanced diagnostic imaging only to be
identified on microscopical examination6-8. In a systematic review of studies examining the cervical spine at
post-mortem of road traffic crash fatalities discrete injuries in the cervical spine, including intervertebral discs
lesions, facet joint fractures and injuries to the joint capsules, synovial folds and ligamentous structures,
were common and many of the discrete injuries remained un-diagnosed on conventional radiological
examination7, which has been supported in subsequent studies9-11. Hence, several studies have found that
minor injuries are often not detected on conventional x-rays, but even CT an MRI have been found to miss
discrete injuries4;6;8;12-18. The highest frequency of injury to the cervical spine facet joints in post-mortem
studies has been reported to be in the lower cervical spine between C4 and C719 20. The purpose of this
study was to investigate whether advanced diagnostic imaging procedures could detect facet joint fractures
and injuries to the synovial folds in the lower cervical spine in a controlled group of post-mortem individuals
using microscopical data as the gold standard.
page 4
Materials and methods
Twenty motor vehicle crash fatalities (cases) and 22 non-traumatic decedents (controls) were included,
consisting of 12 females (median age 40, range 22–49 years) and 30 males (mean age 34.5, range 20–
49 years). From the subjects the lower four cervical spine segments were removed and the facet joints were
examined. Due to post-mortem decomposition two subjects were withdrawn from statistical analysis. The
material has been described in detail elsewhere21. The study was approved by the Scientific Ethics
Committee.
All subjects were examined within 24 hours after autopsy using conventional x-rays, computed tomography
(CT) and magnetic resonance imaging (MRI). Conventional x-ray examination was performed on an
Arcosphere, Arcoma© and consisted of the following projections; AP, lateral and bilateral articular pillar and
oblique views. The film to object distance was one meter, the consol setting of 50 Kv and 32-50 mAs, and
the use of high focus extremity cassettes ensured optimal quality of the images. Computed tomography was
performed on a Phillips© four-slice MX8000 CT scanner. The examination was performed as spiral scanning
of the total volume of the specimen, with a slice thickness of 1,3 mm, increments of 0.6, pitch 0,875, 120 Kv
and 250 mAs per slice using a matrix of 512x512. Axial, coronal, saggital and angled reconstructions were
performed with bone and soft tissue algorithms. Magnetic resonance imaging was performed on a 1.5 T
Signa scanner from General Electrics© using a surface coil. Saggital T1, T2, STIR-sequences, axial T1, T2
and T2*gradient-sequences were performed of the facet joint structures. The majority of sequences were
made with a thickness of 3 mm, spacing 0 and FOV 16x16. The matrix was 512x512 on the saggital
sequences and 256x256 on the remaining.
In the first evaluation of radiological images, two experienced neuroradiologists (obs1 and obs2) scored all
the retrieved images dichotomously, independently and blinded, with regard to general facet fractures and
haemarthrosis/excess fluid in the facet joints. Prior to the first evaluation the observers received no training
or coaching, hence the scoring of observations was based on routine clinical interpretation. During a second
evaluation the observers obtained consensus agreement with regard to the presence or absence of fractures
on all imaging modalities, and haemarthrosis/excess fluid in a facet joint on conventional x-ray and CT-
scanning only. A third evaluation of the MR-images was performed by both observers independently and
blinded with regard to the presence or absence of haemarthrosis/excess fluid in the facet joints only.
Consensus was obtained by the observers, with the variable defined as a joint that on MRI showed focally
page 5
increased signal, with signal differences between adjacent joints on any sequence or relatively increased
signals in all joints.
Each specimen was prepared for microscopical evaluation according to previously published methods21-23,
and the microscopical findings of the 10 μm thick histological sections have been described in detail
elsewhere21;24.
The association of groups was tested with Fisher’s exact test (significance level was p<0.05) and
measurement of agreement between observers was tested with kappa statistics25. All statistical analyses
were performed using Stata© 9 (StataCorp LP, College Station, USA).
page 6
Results
The first evaluation was performed on images from the conventional x-ray examination, CT-scanning and
MRI (Table 1). On the conventional x-ray images, one subject with facet joint fracture was identified by both
observers (1/19 cases) and one subject with facet joint fracture by one observer only (1/19 cases), with a
simple agreement of 97.5% ( = 0.66, 95% confidence interval: 0.37-0.95). On CT-scanning three subjects
with facet joint fractures (3/19 trauma cases) were identified by both observers and two subjects with facet
joint fractures (1/19 cases and 1/21 controls) by one observer only, with an interobserver agreement of
95.0% ( = 0.72, 95% confidence interval: 0.42-1.02). On MRI two subjects with facet joint fractures were
identified by both observers (2/19 cases) and one subject with facet joint fracture by one observer only (1/19
cases), with an interobserver agreement of 97.5% ( = 0.79, 95% confidence interval: 0.49-1.09). No blood
or excess fluid in a joint could be determined on conventional x-ray. One subject (1/19 cases) was scored
positive for bleeding or excess fluid in a facet joint on CT. On MRI three subjects (2/19 cases and 1/21
controls) were scored positive for haemarthrosis/excess fluid in a joint by both observers, and 15 were
scored positive by one observer (7/19 cases and 8/21 controls). The interobserver agreement on the
presence of haemarthrosis/excess fluid in a facet joint on MRI was 62.5% ( = 0.12, 95% confidence interval:
-0.12 to 0.36).
Following the consensus agreement obtained during the second evaluation (Table 1) the presence of
fractures were agreed upon in four trauma cases (4/19) and no controls. Computed tomography was the only
modality capable of identifying all four cases with facet fractures (Figure 1), where MRI identified three and
conventional x-ray one case with facet fractures. Agreement between MRI and CT with regard to subjects
with fractures was 97.5% ( = 0.84, 95% confidence interval: 0.53-1.15), whereas the agreement between
conventional x-ray and CT was 92.5% ( = 0.38, 95% confidence interval: 0.13-0.62). Only on CT there was
statistically significant correlation between subjects with fractures and trauma (p = 0.042, two-sided Fisher’s
exact test). On neither conventional x-ray nor CT was there any positive scoring for the presence of
haemarthrosis/excess fluid in a joint.
The third evaluation (Table 1) revealed haemarthrosis/excess fluid in a joint on MRI in 32 subjects (14/19
cases and 18/21 controls) by both observers, and six were scored positive by one observer (3/19 cases and
3/21 controls). The interobserver agreement of the presence of haemarthrosis/excess fluid in a facet joint on
MRI after the third evaluation was 85.0% ( = 0.31, 95% confidence interval: 0.00-0.62). There was no
page 7
statistically significant correlation between being a trauma case or control subject and haemarthrosis/excess
fluid in a joint on the MRI. Consensus agreement with regard to bleeding on MRI was not obtained.
Microscopical evaluation of the 10 μm thick sections revealed facet fractures in four subjects (4/19 cases)26,
three of whom were identified on neuroradiological evaluation and the remaining case with facet fracture only
identified on histology. Among the four subjects with microscopical fractures a total of 11 unique facet
fractures were identified (Table 2). Furthermore, a fifth subject with a facet fracture identified on CT could not
be confirmed on microscopy. The subject based analysis between the CT consensus findings and the
microscopical findings regarding subjects with fractures resulted in 95% agreement ( = 0.72, 95%
confidence interval: 0.41-1.03) (Table 3) and the correlation between the microscopical findings and CT
consensus findings with regard to unique facet fractures was statistically significant (p < 0.001)(Table 2).
Bleeding in any joint space was present in nine (9/19 cases) and one (1/21 controls) subjects, and
simultaneous bleeding in both synovial folds at any one segment was present in five cases (5/19) and no
controls.
page 8
Discussion
In this post-mortem diagnostic imaging study of the lower cervical spine facet joints, facet fractures were
identified on diagnostic imaging in four of the trauma cases, with CT-scanning being the only imaging
modality capable of identifying all these fractures and a statistically significant correlation between trauma
and fractures. In comparison microscopical evaluation confirmed three of the four facet fractures identified at
CT and revealed another facet fracture not seen on diagnostic imaging. There was substantial agreement
between the CT consensus findings and the microscopical findings with regard to facet fractures. Bleeding in
the facet joints and the facet joint synovial folds could not be confirmed reliably on any diagnostic imaging
procedure, despite microscopical evidence of bleeding in the facet joints.
Fractures of the lower cervical spine facet joints have been described in previous investigations of road
traffic crash fatalities using diagnostic imaging and autopsy data6-8;19;20;27-29. In a post-mortem study of 22
road traffic crash victims, only one fracture of a facet was identified on x-rays and confirmed
microscopically19. Although, x-ray evaluation initially identified four facet fractures these were all read false-
positive due to the lack of microscopical confirmation, which was based on photographic documentation of
the specimens at interval of approximately 1-mm thickness. In a study of 32 post-mortem subjects, two
subjects (2/15 motor vehicle crash fatalities) had suffered fractures to the lower cervical spine facet joints
that could not be identified on conventional x-rays27. More recently, a study of 10 accident victims revealed
two fractures identified on microscopical evaluation in the vicinity of the cervical facet joint (lamina fractures)
that could not be detected on MRI or conventional x-rays, however no distinct fractures to the facets were
identified6. Our study comprised 40 well described subjects (19 road traffic crash fatalities and 21 controls)
that had been investigated in detail using techniques very similar to those utilised in these previous studies.
However, we found an incidence rate of 4/19 subject with facet fractures on the histological sections in the
trauma group which is markedly higher than previously reported, with good agreement between the
observations from CT and microscopy of the 10 μm sections. Furthermore, we found a total of 11 unique
facet fractures on microscopy, divided among these four subjects, of which seven were not reported on the
CT evaluation, and a fifth subject with potential fractures was identified on CT that could not be verified on
microscopy (Table 2). This may suggest that the previous studies6;19;27 of mixed trauma mechanisms (falls,
sporting injuries and different types of road traffic crashes, e.g. motorcycle crashes and pedestrian injuries)
have different outcomes with regard to the incidence rate of facet joint injuries due to differences in the
page 9
mechanism of trauma, which may be very different from passenger car crashes. It also suggests that, when
present, facet fractures are more often affecting several facets rather than solitary facets. None of these
findings could be confidently confirmed on the stereomicroscopic evaluation of the 3-mm thick slices, since
the results from this evaluation showed no correlation with trauma or the microscopical findings21.
Haemarthrosis of the cervical spine facet joints have been described in post-mortem studies of road traffic
crash victims using histological and/or microtomal methods6-8;19;20;27;28. In a study of 10 accident victims
(unknown proportion of road traffic crash victims), haemarthrosis was reported in 10 joints on microscopical
evaluation, with only six of the 10 joints with haemarthrosis identified on MRI, which was conducted
retrospectively6. Besides this study, no other forensic diagnostic imaging studies have described this
condition in detail. Our results support these finding6, in that the presence of haemarthrosis or bleeding in the
synovial folds cannot reliably be established based on diagnostic imaging procedures, despite microscopical
evidence of bleeding in one or more joints in almost half the trauma cases and simultaneous bleeding in the
segmental synovial folds in a quarter of the trauma cases21. Numerous studies have been published
investigating the contributions from MRI and CT in forensic settings, and it can be anticipated that the
increasing use of these modalities gradually will replace the role of conventional x-rays in the screening of
the deceased during autopsy2-4;8. However, in the study of the cervical spine of road traffic crash fatalities
only few studies have utilised advanced diagnostic imaging procedures2;6;8;28;29, whereas a substantial
number of studies have included conventional x-ray evaluation7. In a large post-mortem study of 109 trauma
fatalities, a substantial number of injuries were missed on conventional x-ray evaluation although the exact
detection rate of facet joint fractures was not reported20. Except for one recent study6, the majority of
previous post-mortem studies examining the cervical spine have not attempted to confirm microscopical or x-
ray findings with CT or MRI19;20;27. We found that only one of the four fractures identified on CT could be
visualised on conventional x-ray evaluation, which suggests that the previous studies utilizing conventional x-
rays only may have under-reported the true incidence of fractures that potentially could have been detected
on advanced diagnostic imaging procedures. Similarly, our results supports other studies where CT has
been shown to be the most reliable diagnostic imaging procedure with regard to detecting fractures of the
cervical spine2;9-11;18. Notwithstanding this fact, a recent post-mortem forensic neuroimaging study, reported
that CT and MRI missed two (2/2) atlas C1 fractures, two fractures at axis C2 (2/4) on CT and three fractures
at axis C2 (3/4) on MRI, with the injuries being confirmed on autopsy2. With regard to soft tissue lesions in
page 10
the facet joints, such as bleeding in the joint space and the synovial folds, we found, in accordance with
other studies, that the presence and structural integrity of synovial folds of the lower cervical spine could not
be determined reliably on neither conventional x-ray, CT or MRI6;8;12;30. Recently, however, the cervical spine
facet joint folds have clearly been visualised on MRI, although this required a high energy-field 3.0 Tesla MRI
unit, with long acquisition time, limited field of view and a small specimen size31. In our study we used a 1.5
Tesla MRI unit and the protocols used did not allow adequate resolution, and the slight interobserver
agreement is therefore probably more a consequence of technical limitations rather that academic2;31. With
increasing availability of high energy-field MR-scanners reliable evaluation of the structural integrity of the
synovial folds and identification of bleeding in the joint spaces and the synovial folds becomes increasingly
possible. We found good indication for utilising CT and to a certain extent MRI for the purpose of identifying
fractures of post-mortem cervical spine facet joints. However, we did not find support in our study for use of
these modalities for the purpose of identifying bleeding in facet joints or synovial folds.
There is a scarcity of publications addressing the reliability and validity of forensic diagnostic imaging
evaluation. No previous publication have described the degree of inter- and intraobserver agreement nor the
exact effect of training of observers with regard to scoring of forensic radiological images, although recent
comments in this regard have been proposed2. In comparison, a recent clinical study evaluated the reliability
of in vivo CT-scanning, in which a clinical classification system for lower cervical spine injuries based on
conventional radiology and CT-scanning was proposed based on excellent intra- and interobserver
agreement32. We found substantial interobserver agreement with regard to facet fractures, however the
interobserver agreement of the MRI evaluation regarding the presence of haemarthrosis/excess fluid in a
facet joint was slight despite training of the observers with regard to scoring this variable. Actually, the
training towards scoring the facet joints on MRI with regard to haemarthrosis/excess fluid in a joint caused a
significant increase in the number of joints positive for this variable which had no correlation to cases or
controls, suggesting either improper definition of the variable or clinically irrelevant structural changes in
these joints at post-mortem.
Histological procedures have the advantages of allowing microscopical evaluation of relevant sections as
well as increasing sensitivity by adequate staining procedures. However, similar to previous studies6;20;27, the
sensitivity towards identifying very discrete fractures could be limited by the section thickness, which was 3-
mm in our study. Linear lesions, parallel with the parasaggital line of sectioning, and lesions smaller than 3
page 11
millimetres could potentially remain undetected on the microscopical examination21. Furthermore, the long
fixation time in alcohol and the embedding of the un-decalcified specimens in MMA caused the erythrocytes
to appear less vividly on the consequent un-deplastified staining. This may explain why some fractures were
difficult to identify on microscopical evaluation. By reducing the section thickness more injuries would be
detectable on microscopical examination. Likewise, increasing the technical specifications of the
radiographic equipment and improving the radiologists knowledge of post-mortem anatomical changes
should improve the sensitivity of these procedures2.
Advanced diagnostic imaging procedures, in particular CT, did detect facet joint fractures in a substantial
proportion of the lower cervical spine facet joints of post-mortem individuals killed in a motor vehicle crash
and showed good correlation with findings from microscopical evaluation. The findings confirm that discrete
osseous injuries are common in the facet joints following fatal road traffic crashes, and that not all discrete
facet fractures are identified on diagnostic imaging procedures. Furthermore, bleeding in the cervical facet
joints and synovial folds could not be determined reliably on any diagnostic imaging modality although
microscopical evaluation revealed bleeding in a large proportion of the facet joints and synovial folds of the
motor vehicle crash fatalities. This study emphasizes the need for scientific evidence of validity and reliability
of advanced diagnostic imaging procedures in forensic settings, in particular with regard to non-fatal soft
tissue lesions, and until such evidence has been produced these procedures must be considered adjunct
techniques to the post-mortem autopsy.
page 12
Acknowledgements
This study has complied with the national laws on scientific research projects and has been approved by the
Scientific Ethics Committee, Aarhus County. The study was generously supported by the European
Chiropractors Union Research Fund Grant no. A.03-5, Switzerland, the Foundation for the Advancement of
Chiropractic Research, Denmark and the University of Aarhus Research Foundation, Denmark. The authors
would like to acknowledge the original contributions from Professor DMSc. Flemming Melsen†, the timely and
professional cooperation of the staff at the Institute of Forensic Medicine, University of Aarhus and the
Department of Neuroradiology, Aarhus Sygehus. Furthermore, we acknowledge the efforts of Rita Ullerup for
the careful preparation of the histological sections and the neuroradiological observations made by senior
consultant Vibeke Fink-Jensen.
page 13
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page 14
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cervical trauma. J Trauma 1992;33:698-708.
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page 15
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spine facet joints. (Submitted) 2007.
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page 16
Figure 1 3-D reconstruction of CT-images of a facet joint fracture in a motor vehicle crash fatality
A fracture (arrow) is localised in the superior articular process of C6 on the left.
page 17
Figure 2 Histological microimage of a fracture of a lower cervical spine facet joint following a fatal motor
vehicle crash
Overview of a parasaggital histological section through the lower cervical spine facet joints shows a
fracture (F) of the superior articular process (SAP) of C6 on the left, and the shaded area is visualised in
a close-up illustrating the fractures (F) and haemarthrosis in the joint space (JS), original magnification
1.25x, Masson Goldner-Trichrome.
page 18
Tabl
e 1
Eva
luat
ions
of t
he n
euro
radi
olog
ical
imag
es w
ith re
gard
to fr
actu
res
and
haem
arth
rosi
s/ex
cess
flui
d in
a fa
cet j
oint
X-
ray
CT
MR
I
Cas
es
obs1
-obs
2 fra
ctur
e ha
em.
fract
ure
haem
. fra
ctur
e ha
em.
1. e
valu
atio
n (n
=19)
0-
0 17
19
15
18
16
10
0-
1 1
0 0
1 0
5
1-
0 0
0 1
0 1
2
1-
1 1
0 3
0 2
2
C
ontr
ols
0-0
21
21
20
21
21
12
(n
=21)
0-
1 0
0 0
0 0
8
1-
0 0
0 1
0 0
0
1-
1 0
0 0
0 0
1
2.
eva
luat
ion
Cas
es
0-0
18
19
15
19
16
(n
=19)
0-
1 0
0 0
0 0
1-0
0 0
0 0
0
1-
1 1
0 4
0 3
-
Con
trol
s 0-
0 21
21
21
21
21
(n=2
1)
0-1
0 0
0 0
0
1-
0 0
0 0
0 0
1-1
0 0
0 0
0
-
3. e
valu
atio
n C
ases
0-
0 2
(n
=19)
0-
1 2
1-0
1
1-
1
- -
-
14
Con
trol
s 0-
0 0
(n
=21)
0-
1 1
1-0
2
1-
1
- -
-
18
fract
ure:
frac
ture
of a
cer
vica
l spi
ne fa
cet j
oint
ha
em.:
haem
arth
rosi
s/ex
cess
flui
d in
a c
ervi
cal s
pine
face
t joi
nt
obs1
: obs
erve
r one
ob
s2: o
bser
ver t
wo
page 19
Table 2 Subjects scoring positive for facet fracture of either histology or CT consensus
Subject # 10 μm histology CT consensus
22 (case) C5 right IAP fracture -
25 (case)
C5 left IAP fracture
C6 left SAP fracture C6 left IAP fracture
C7 left SAP fracture
C6 right SAP fracture
-
C6 left SAP fracture -
-
-
39 (case)
Th1 left SAP fracture -
C5 right IAP fracture
Th1 left SAP fracture C7 left IAP fracture
-
53 (case)
C7 left IAP fracture
C6 right IAP fracture C7 right SAP fracture
-
C6 right IAP fracture C7 right SAP fracture
24 (case) - Th1 left SAP fracture
The total number of unique facets is 16 per subject, except for one subjects with a bloc vertebra with 12 facets (636 facets in total among the 40 subjects)
Correlation per unique facet fracture (Fishers exact test): risk ratio 60 (95% confidence interval: 24 - 152, p < 0.001)
SAP: superior articular process
IAP: inferior articular process
page 20
Table 3 Agreement between CT consensus and histological findings regarding facet fracture
Subjects (n = 40) CT – 10 μm Fracture
0 - 0 35
0 - 1 1
1 - 0 1
1 - 1 3 ( = 0.72, 95% confidence interval: 0.41-1.03)
CT: computed tomography scanning
10 μm: microscopy of 10 μm thick histological sections
Fracture: cervical spine facet joint fractures
page 21
Table 4 Subject based description of facet fractures on radiology and histology
RADIOLOGY (CONSENSUS) HISTOLOGY
Subject # Age Gender Facet facture
on X-ray Facet facture
on CT Facet facture
on MRI Facet fracture on
10 μm 26 21 M No No No No 24 22 F No Yes Yes No 35 33 M No No No No 14 20 M No No No No 20 29 M No No No No 25 36 M Yes Yes Yes Yes 42 29 M No No No No 47 23 F No No No No 21 31 F No No No No 13 34 M No No No No 17 45 F No No No No 19 35 M No No No No 22 20 M No No No Yes 36 29 M No No No No 46 37 M No No No No 53 31 M No Yes Yes Yes 39 41 M No Yes No Yes 34 47 M No No No No 28 38 M No No No No 19 cases 1 4 3 4 16 39 F No No No No 48 46 F No No No No 12 41 M No No No No 29 34 F No No No No 43 33 M No No No No 30 43 F No No No No 38 49 M No No No No 18 37 M No No No No 45 35 M No No No No 51 23 M No No No No 15 32 M No No No No 23 37 M No No No No 31 31 M No No No No 44 40 M No No No No 52 48 M No No No No 50 41 F No No No No 49 41 F No No No No 40 27 F No No No No 54 22 M No No No No 37 49 F No No No No 33 35 M No No No No 21 controls 0 0 0 0
Gender: male (M), female (F)
Pathoanatomy of the lower cervical spine facet joints in motor
vehicle crash fatalities
Lars Uhrenholt1,2,3, Annie Vesterby Charles1,3, Ellen Hauge3,4, Markil Gregersen1
1 Institute of Forensic Medicine, University of Aarhus, Denmark
2 Nordic Institute of Chiropractic and Clinical Biomechanics, Part of Clinical Locomotion Science, Odense,
Denmark
3 Research Unit of Rheumatology and Bone Biology, Aarhus University Hospital, Aarhus Sygehus (NBG),
Denmark
4 Department of Rheumatology, Aarhus University Hospital, Aarhus Sygehus (NBG), Denmark
Corresponding author:
Lars Uhrenholt
Institute of Forensic Medicine
University of Aarhus
Brendstrupgaardsvej 100, 8200 Aarhus N, Denmark
E-mail: lu@forensic.au.dk
Facsimile: 45-86125995
Phone: 45-89429800
PAPER II
page 2
Acknowledgements
The authors would like to acknowledge the original contributions from Professor DMSc. Flemming Melsen†,
the professional cooperation of the staff at the Institute of Forensic Medicine, University of Aarhus. The
efforts of Rita Ullerup for the careful preparation of the histological sections are greatly appreciated. The
study received support from the European Chiropractors Union Research Fund Grant no. A.03-5,
Switzerland, the Foundation for the Advancement of Chiropractic Research, Denmark and the University of
Aarhus Research Foundation, Denmark.
page 3
Abstract
In decedents from motor vehicle crashes, lesions to the cervical spine facet joints have previously been
described that were non-lethal. The aim of this study was to conduct a detailed examination of the lower
cervical spine facet joints in a population of motor vehicle crash victims and controls using comparable data
from medicolegal autopsy, stereomicroscopy and histological evaluations. Injuries to the cervical spine facet
joints were common and included facet fractures, haemarthrosis and bleeding in the synovial folds. The
majority of injuries could not be verified by stereomicroscopic evaluation, and conventional autopsy
procedures did not reveal any of the injuries to the facet joints. Despite the presence of these
pathoanatomical lesions in road traffic crash fatalities their potential clinical implications in survivors from
motor vehicle crashes are unknown.
page 4
Introduction
Road traffic crashes remain responsible for the death of more than 40.000 people in Europe annually, and in
addition to the fatalities there is an estimated 3.5 million casualties per year in Europe with estimated costs
of 250 billion Euro1;2. Non-fatal injuries to the cervical spine facet joints have been related to the clinical
picture of chronic neck pain following road traffic crashes which is responsible for substantial morbidity3-6.
However, the aetiology of chronic neck pain with regard to which somatic structures may be injured,
damaged or diseased remains unclear. The limited anatomical knowledge of non-fatal injuries in the cervical
spine facet joints is related to often inconclusive clinical diagnostic imaging studies despite subjective
complaints from the patients. Despite advancements in the field of diagnostic imaging procedures, including
improved resolution of computed tomography and magnetic resonance imaging, discrete injuries may remain
undetected on these investigations7-9. Since histological procedures are not viable for in vivo human studies,
post-mortem studies have been conducted in order to examine the potential anatomical basis for sustained
neck pain following trauma. In several post-mortem studies, non-fatal lesions in the cervical spine of road
traffic crash fatalities have been identified, including injuries to the facet joint capsules, folds and articular
surfaces9-14. Only few studies, however, have evaluated homogenous study groups including details of the
mechanism of trauma, cause of death and controls subjects. Therefore, the extent of non-fatal injuries to the
cervical spine facet joints with regard to types of lesions and anatomical locations is unknown in both clinical
settings and post-mortem material.
The aim of this study was to examine the lower cervical spine facet joints in a population of motor vehicle
crash fatalities compared with an age-matched control group for the presence of cervical spine facet joint
injuries using comparable data from medicolegal autopsy, stereomicroscopy and histological evaluations
using the histological findings as gold standard.
page 5
Materials and methods
Materials
Forty-two subjects were examined at medicolegal autopsy within 1-5 days (median 3 days) after death and
included in this study. During autopsy the lower four cervical vertebral segments (C4-C7) including
paravertebral muscles were removed en bloc, from twelve females (median age 40 years, range 22–49) and
30 males (median age 34.5 years, range 20–49 years). Twenty died in a passenger car crash (cases) and 22
died due to non-traumatic causes (controls). Subjects were excluded if there was evidence of previous
history of drug and/or alcohol abuse, previous cervical spine injury, and extensive post mortem
decomposition. Two subjects (one case and one control) were excluded from statistical analysis due to
extensive decomposition causing generalized tissue damage. The study was approved by the Scientific
Ethics Committee.
Methods
The specimens were fixated in 70 % ethanol for a minimum of five weeks with hemisection in the median
plane after two weeks, followed by one week in 96 % ethanol under vacuum conditions fixation and a final
week in 99 % ethanol. Then each specimen was embedded in liquid methylmethacrylate (MMA) and
dibutylphtalate (a softener) in a refrigerator for six weeks, after which percadox (a catalyst) was added to
complete polymerisation and hardening into a plastic bloc. From a random central starting point, each
plastic bloc was sawed by serial sectioning, into approximately seven 3-mm thick parasaggital slices using a
precision guided bandsaw (Femi©, Bologna, Italy), which ensured exact thickness of the slices with a tissue
loss of approximately 1 mm per slice. Each 3-mm thick slice was examined using a stereomicroscope and
scored with reference to damage of the facet cartilage and/or bone, bleeding in a joint, the presence of
synovial folds and injury to the folds.
The 3-mm thick slices containing facet joints were re-embedded in MMA. Using a heavy-duty microtome (SM
2500, Leica©) two consecutive histological sections of 10 μm thickness were produced from each bloc,
stained with Masson Goldner-Trichrome, and mounted un-deplastified on glass slides. All facet joints on
histological sections were examined by light microscopy using a BX51, Olympus© microscope. An average of
45.8 unique observations per subject (2.9 observations per unique facet) were made including the scoring of
predetermined variables; articular facet fractures, osteochondral fissures with or without bleeding, bleeding in
page 6
the joint space, bleeding in the anterior, posterior or both synovial folds, bleeding in the underlying bone and
the integrity of the anterior and posterior folds.
Fisher’s exact test was used to examine the significance of association between categorical variables and
Chi-squared test was used to examine the correlation of the number of disrupted folds per subject
(case/control) versus exposure to trauma. Agreement between diagnostic methods was examined with
kappa statistics. The significance level was p<0.05. All statistical analyses were performed using Stata© 9
(StataCorp LP, College Station, USA).
page 7
Results
Autopsy findings
The medicolegal autopsy identified no injuries to the lower cervical spine facet joints (Table 1). In the trauma
group seven unique fractures in cervical spine vertebral bodies were identified in four subjects (4/19 cases),
with one classified as a disco-vertebral avulsion fracture at C6-C7, and the remaining fractures situated at or
above C3. Skull fractures were identified in eight cases (8/19). There were significant injuries to cranial
organs in 11/19 cases, thoracic organs in 18/19 cases, and abdominal organs in 17/19 cases. Injuries to the
spleen and liver affected 15/19 cases and injuries to the lungs affected 15/19 cases. The primary cause of
death in the trauma group was multiple injuries in 10/19 cases and bleeding in 6/19 cases. In eighteen of the
cases (18/19 cases) the decedent was the driver of a passenger car and the remaining one case (1/19
cases) was a passenger in a motor vehicle. In the control group subjects (n=21) there were neither injuries to
the musculoskeletal system nor traumatically induced organic injuries. The most common causes of death
among the control group subjects was cardiovascular disease in 12/21 subjects. Toxicological evaluation
revealed a blood alcohol concentration (BAC) > 0.8 mg/ml in eight subjects (5/19 cases and 3/20 controls
tested), with four drivers (4/18 drivers) killed in a motor vehicle crash being under the influence of alcohol
(BAC > 0.8 mg/ml in three cases and alcohol concentration in the vitreous humor of 2.4 mg/ml in one case)
(Table 2). Medication was found in four subjects (3/9 cases tested and 1/10 controls tested) and narcotics
were found in three subjects (1/9 cases tested and 2/10 controls tested).
Stereomicroscopy of the 3-mm thick slices
On the stereomicroscopy of the 3-mm slices damage to the facet cartilage and/or bone was present in 10
subjects (3/19 cases and 7/21 controls) and the presence of damage could not be evaluated in 29 subjects
(15/19 cases and 14/21 controls). There was no significant correlation between exposure of trauma and the
presence of damage to the facet cartilage and/or bone (p = 0.28). Bleeding in a joint was present in 3
subjects (3/19 cases), which did not correlate with exposure to trauma (p = 0.10), and the presence of
bleeding in a joint could not be evaluated in 26 subjects (12/19 cases and 14/21 controls). Synovial folds
were found in 21 subjects (21/40) and could not be evaluated in 21 subjects (10/19 cases and 11/21
controls) and no injuries to the folds were detected.
page 8
Light microscopy of the 10 μm thick sections
Light microscopy of the 10 μm sections initially identified facet fractures (Figure 1) in three subjects (3/19
cases) however, after review of journals with “possible fractures” a fourth case with facet fractures was
identified. The histological findings of a facet fracture correlated with the exposure to trauma (p < 0.05)
(Table 3). Osteochondral fissures without blood were detected in all subjects (n = 40) affecting on average
59 % of the facets among the cases, and 57 % of the facets among the controls, whereas osteochondral
fissures with bleeding were identified in three cases (3/19) and no controls (p < 0.01) (Table 3). Blood in the
underlying bone was present in 32 subjects (15/19 cases and 17/21 controls). Bleeding in any joint space
(haemarthrosis) was present in nine cases (9/19) and one control subject (1/21) (Figure 2). There was
significant correlation between bleeding in any joint and exposure to trauma (p < 0.01), between bleeding in
any joint and the presence of a fracture on histological evaluation (p < 0.05) and between bleeding in any
joint and bleeding in both synovial folds at the same segment (p < 0.001).
Bleeding in any fold was present in 11 cases (11/19) and seven controls (7/21) and was not statistically
significant (p = 0.20), however simultaneous bleeding in both folds at any one segment was present in five
cases (5/19) and no controls (p < 0.05) (Figure 3). There was significant correlation between simultaneous
bleeding in both folds at one spinal segment and the presence of a fracture (p < 0.01). A total of 27 subjects
(15/19 cases and 12/21 controls) had a disrupted anterior fold and thirty-three subjects (18/19 cases and
15/21 controls) had a disrupted posterior fold with no significant correlation to trauma. However, disruption of
the posterior fold combined with bleeding in the same fold at the same level revealed five trauma cases
(5/19) and no controls (p < 0.02). Analysis of the incidence rates of disrupted folds per subject (using Chi-
squared test) revealed a risk ratio of 1.8 (95 % confidence interval: 1.5 – 2.2, p < 0.001) and 1.8 (95 %
confidence interval: 1.4 – 2.2, p < 0.001), for disruption of the anterior and posterior fold respectively with
regard to exposure to trauma (Table 3). Simultaneous disruption of both folds at any one segment was found
in 15 subjects (10/19 cases and 5/21 controls, p = 0.10), and if combined with bleeding in any of the same
two folds or both, seven cases (3/19) and no controls scored positive (p < 0.01).
There was no correlation between the stereomicroscopy and histological findings concerning damages to the
facet cartilage and/or bone or the synovial folds. It is worth noticing that none of the injuries to the facet joints
were observed during the autopsy.
page 9
Discussion
The detection of non-fatal injuries to the cervical spine facet joints was not reported equally among the
diagnostic methods used in this study. Based on conventional autopsy detailed description of fatal injuries
could be performed, however no injuries to the cervical spine facet joints were detected. Results from the
stereomicroscopic evaluation of the 3-mm slices did not reach statistically significant correlation between any
of the parameters evaluated. In contrast, microscopical evaluation of the 10 μm thick sections revealed
statistically significant correlations between exposure to trauma, and the presence of non-fatal articular facet
fractures, disruption of the folds, bleeding in the facet joints and simultaneous bleeding in the both folds.
In this study the most common cause of death in the trauma group was multiple injuries, and the high
incidence rates of skull fractures and organic injuries were all in concurrence with previously reported injuries
in road traffic crash fatalities15. Forensic toxicology revealed that four of the 18 drivers killed were under the
influence of alcohol during the time of the crash which is similar to previously reported figures of 20-30 % of
decedents from fatal road traffic crashes having BAC values above 0.5 mg/ml16-18. Similarly we found one
trauma case who tested positive for drugs which also supports previous reports of drugs in road traffic crash
fatalities17. The medicolegal autopsy did not identify injuries in the cervical spine facet joints despite
histological and neuroradiological evidence of injuries. However, this is likely due to the choice of autopsy
technique utilized (i.e. anterior approach) which does not allow detailed description of the posterior elements
of the cervical spine. Hence, the poor sensitivity towards identifying injuries in the facet joints is not
surprising and concurs with other studies reaching the same conclusions regarding standardised
autopsies7;9-11;14;19.
Several post-mortem studies of trauma fatalities have reported subjects with fractures of the lower cervical
spine facet joints similar to those identified in our study9-12;14;19-21. However, focusing on studies examining
road traffic victims, the 1/22 and 1/15 traffic accident victims sustaining lower cervical spine facet joint
fractures, examined in the studies by Jónsson et al12 and Taylor and Twomey10 respectively, is significantly
lower than our findings of facet fractures in 4/19 trauma cases. The differences between the reported figures
may be due to the primary focus on facet joint injuries in our study in contrast to the previous studies
examining the whole cervical spine. Furthermore, our material exclusively involved subjects killed in motor
vehicle crashes which indicate that all the decedents have been exposed to forces of significant magnitudes.
The low number of subjects examined in all the studies as well as technical issues such as the histological
methods utilized could influence the results. Osteochondral fissures without bleeding were non-specific
page 10
findings and in many cases likely due to artefacts caused by the microtome sectioning. In contrast, bleeding
was only identified in three subjects (3/19 cases) and consequently recorded as a fractures.
Haemarthrosis of the cervical spine facet joints have been described in post-mortem studies of road traffic
crash victims using histological and/or microtomal methods9-12;14;19;20. However, due to the nature of the
different methods used in these studies the presence of erythrocytes in the joint cavities have not been
clearly demonstrated in all studies, in particular not in studies utilising photographic documentation of the
remaining tissue bloc after removal of micrometer thick sections. In our study the erythrocytes were, after
and in comparison with blood vessel content, identified as pale cell ghosts in a honeycomb pattern. By this
definition, haemarthrosis was identified in almost half the trauma cases with statistical significance. Similarly,
a recent study investigated 10 consecutive trauma fatalities, with no reference to the proportion of traffic
crash victims in the material and the specific segments examined, and found haemarthrosis in the facet
joints in 6 of the 10 cases based on microscopy of 3-mm thick slices and in some cases histopathologic
examination19. In another post-mortem study haemarthrosis was present in six of 15 trauma cases, with only
three affecting the lower cervical spine facet joints below C410. However, the exact manner of identification of
bleeding within the joints was not described in detail in any of these studies and combined with our finding
that stereomicroscopic evaluation of 3-mm thick slices do not justify reliable conclusions regarding the
presence of bleeding in the facet joints we find the previously reported results questionable.
Although there were a higher number of subjects with disrupted folds in the trauma group than the control
group, statistical significance was only present when analysis of the individual number of disrupted folds per
subject was performed. This revealed that the posterior fold was at higher risk of injury during a fatal road
traffic crash compared to the anterior counterpart. Similarly, simultaneous bleeding in the anterior and
posterior fold was present in several trauma cases only which indicates significant trauma. No previous
publications have reported specific subject based incidence rates for the occurrences or locations of
bleeding in the folds, although the lesions have been reported9-14;19. The presence of erythrocytes in and the
disruption of synovial folds in a number of the control group subjects suggest that artefacts may be
introduced at post-mortem.
Despite good homogeneity (all cases were passenger car occupants, the age ranges were restricted to 20-
49 years and the controls were non-traumatised) and detailed multifaceted evaluation the study population,
the gold standard chosen did not have the possibility of identifying all lesions. Facet fractures parallel to the
line of sectioning would not necessarily appear on the histological sections and discrete fractures could
page 11
potentially be present inside the 3-mm slices but outside the area of microtomal sectioning. Furthermore,
prolonged ethanol fixation and staining of un-deplastified histological sections may have caused the poor
visualisation of erythrocytes in lesions sites and thereby underestimation of bleeding.
The findings of non-fatal disruption with or without bleeding in a significant number of folds suggest that such
injuries may be present in injured survivors from severe road traffic crashes possibly acting as a source of
pain mediated through pain pathways. We furthermore observed haemarthrosis which may have clinical
significance in the light of recent studies finding that even brief exposures to blood may have detrimental
long-lasting effect on the cartilage, by inhibiting the proteoglycan synthesis, thereby predisposing to
premature degeneration22-25. Acute synovitis after haemarthrosis and/or cartilage damage after trauma has
also been described in the literature22;25, which also may have clinical implications for development of neck
pain following adequate trauma. The possibility of degradation of cartilage matrix and subsequent
development of degenerative changes in articular structures may correlate with diagnostic imaging findings
of increasing osteoarthrosis in road traffic trauma patients years after the injury26-28, although opinions are
divergent27;29. The true incidence rates of bleeding in cervical spine facet joints and folds after survivable
road traffic crashes have not been reported and the potential clinical implications are inconclusive.
page 12
Conclusions
In this controlled study of motor vehicle crash fatalities, non-fatal injuries to the lower cervical spine facet
joints were a common finding, including facet fractures, haemarthrosis, disruption and bleeding in the
synovial folds. The majority of lesions were not present on stereomicroscopic evaluation, and conventional
autopsy procedures did not reveal any of the injuries. The utilisation of advanced imaging modalities as well
as specialized autopsy techniques should be encouraged in forensic settings in order to increase the
sensitivity towards identifying such discrete injuries. The clinical implications of the lesions identified in these
subjects are unknown, however, it is possible that discrete injuries similar to those identified in this study will
be present in a number of survivors from severe motor vehicle crashes.
page 13
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http://www.erso.eu/safetynet on May 27, 2007.
3. Cavanaugh JM, Lu Y, Chen C et al. Pain generation in lumbar and cervical facet joints. J Bone Joint
Surg.Am. 2006;88 Suppl 2:63-7.
4. Barnsley L. Percutaneous radiofrequency neurotomy for chronic neck pain: outcomes in a series of
consecutive patients. Pain Med. 2005;6:282-6.
5. Banic B, Petersen-Felix S, Andersen OK et al. Evidence for spinal cord hypersensitivity in chronic pain
after whiplash injury and in fibromyalgia. Pain 2004;107:7-15.
6. Curatolo M, rendt-Nielsen L, Petersen-Felix S. Central hypersensitivity in chronic pain: mechanisms
and clinical implications. Phys.Med.Rehabil.Clin.N.Am. 2006;17:287-302.
7. Uhrenholt L, Nielsen E, Vesterby Charles A et al. Imaging occult lesions in the cervical spine facet
joints. (Submitted) 2007.
8. Holmes JF, Mirvis SE, Panacek EA et al. Variability in computed tomography and magnetic resonance
imaging in patients with cervical spine injuries. J.Trauma 2002;53:524-9.
9. Uhrenholt L, Grunnet-Nilsson N, Hartvigsen J. Cervical spine lesions after road traffic accidents: a
systematic review. Spine. 2002;27:1934-41.
10. Taylor JR, Twomey LT. Acute injuries to cervical joints. An autopsy study of neck sprain. Spine
1993;18:1115-22.
11. Taylor JR, Taylor MM. Cervical spinal injuries: an autopsy study of 109 blunt injuries. J
Musculoskeletal Pain 1996;4:61-79.
page 14
12. Jonsson H, Jr., Bring G, Rauschning W et al. Hidden cervical spine injuries in traffic accident victims
with skull fractures. J.Spinal Disord. 1991;4:251-63.
13. Schonstrom N, Twomey L, Taylor J. The lateral atlanto-axial joints and their synovial folds: an in vitro
study of soft tissue injuries and fractures. J.Trauma 1993;35:886-92.
14. Uhrenholt L, Nielsen E, Vesterby A et al. Detailed examination of the lower cervical spine facet joints in
a road traffic crash fatality - a case study. IRCOBI (annual proceedings) 2005;paper 701;411-414.
15. Saukko P, Knight B. Knight's Forensic Pathology. 3rd. ed. London, UK: Arnold, a member of the
Hodder Headline Group, 2004.
16. Hansen AC, Kristensen IB, Dragsholt C et al. Alcohol and drugs (medical and illicit) in fatal road
accidents in a city of 300,000 inhabitants. Forensic Sci.Int. 1996;79:49-52.
17. Drummer OH, Gerostamoulos J, Batziris H et al. The incidence of drugs in drivers killed in Australian
road traffic crashes. Forensic Sci.Int. 2003;134:154-62.
18. European Road Safety Observatory (2006). Alcohol. Accessed at http://www.erso.eu/safetynet on
May 27, 2007.
19. Stäbler A, Eck J, Penning R et al. Cervical spine: postmortem assessment of accident injuries--
comparison of radiographic, MR imaging, anatomic, and pathologic findings. Radiology 2001;221:340-
6.
20. Bergstrom K, Nyberg G, Pech P et al. Multiplanar spinal anatomy: comparison of CT and
cryomicrotomy in postmortem specimens. AJNR Am.J.Neuroradiol. 1983;4:590-2.
21. Rauschning W, McAfee PC, Jonsson H, Jr. Pathoanatomical and surgical findings in cervical spinal
injuries. J.Spinal Disord. 1989;2:213-22.
22. Roosendaal G, Vianen ME, Marx JJ et al. Blood-induced joint damage: a human in vitro study. Arthritis
Rheum. 1999;42:1025-32.
page 15
23. Hooiveld M, Roosendaal G, Vianen M et al. Blood-induced joint damage: longterm effects in vitro and
in vivo. J Rheumatol. 2003;30:339-44.
24. Hooiveld M, Roosendaal G, Wenting M et al. Short-term exposure of cartilage to blood results in
chondrocyte apoptosis. Am.J Pathol. 2003;162:943-51.
25. Jansen NW, Roosendaal G, Bijlsma JW et al. Exposure of human cartilage tissue to low
concentrations of blood for a short period of time leads to prolonged cartilage damage: an in vitro
study. Arthritis Rheum. 2007;56:199-207.
26. Hohl M. Soft-tissue injuries of the neck in automobile accidents. Factors influencing prognosis. J Bone
Joint Surg.Am. 1974;56:1675-82.
27. Gore DR, Sepic SB, Gardner GM et al. Neck pain: a long-term follow-up of 205 patients. Spine
1987;12:1-5.
28. Watkinson A, Gargan MF, Bannister GC. Prognostic factors in soft tissue injuries of the cervical spine.
Injury 1991;22:307-9.
29. Robinson DD, Cassar-Pullicino VN. Acute neck sprain after road traffic accident: a long-term clinical
and radiological review. Injury 1993;24:79-82.
page 16
Figure 1 Fractures of the opposing cervical spine facets in a motor vehicle crash fatality
Overview of the joint, inferior articular process (IAP), superior articular process (SAP), joint space (JS)
and facet fracture (F), original magnification x1.25, Masson Goldner-Trichrome
page 17
Figure 2 Haemarthrosis in a cervical spine facet joint in a motor vehicle crash fatality
Large overview of the joint, inferior articular process (IAP), superior articular process (SAP), synovial fold
(SF), joint space (JS), original magnification x1.25, Masson Goldner-Trichrome, and a close-up of
shaded area illustrating bleeding in the joint space (B), original magnification x4, Masson Goldner-
Trichrome
page 18
Figure 3 Injuries to the cervical spine facet joint in a motor vehicle crash fatality
General overview of the joint, inferior articular process (IAP), superior articular process (SAP), synovial
fold (SF), joint space (JS), original magnification x1.25, Masson Goldner-Trichrome, and close-up of
shaded areas illustrating bleeding in the fold (BF) and joint (B), and an osteochondral fracture (F),
original magnification x4, Masson Goldner-Trichrome
Tabl
e 1
Det
aile
d de
scrip
tion
of th
e au
tops
y fin
ding
s
Subj
ect
Age
Gen
der
Circ
umst
ance
s Pr
imar
y ca
use
of d
eath
Sk
ull
frac
ture
C
ervi
cal s
pine
ve
rteb
ral f
ract
ure
Thor
acic
spi
ne,
lum
bar s
pine
and
/or
pelv
ic fr
actu
res
Extr
emity
frac
ture
s In
trac
rani
alor
gan
in
jurie
s Th
orac
ic o
rgan
in
jurie
s Ab
dom
inal
org
an
inju
ries
26
21
M
Pass
enge
r, R
TC
Mul
tiple
trau
mat
ic in
jurie
s Ye
s N
o Pe
lvis
H
umer
us, f
emur
Ye
s Ye
s Ye
s
24
22
F D
river
, RTC
M
ultip
le tr
aum
atic
inju
ries
Yes
No
No
ulna
, fem
ur a
nd ti
bia
Yes
Yes
Yes
35
33
M
Driv
er, R
TC
Blee
ding
, hae
mot
hora
x, ru
ptur
e th
orac
ic a
orta
N
o N
o N
o tib
ia, p
edis
N
o Ye
s Ye
s
14
20
M
Driv
er, R
TC
Mul
tiple
trau
mat
ic in
jurie
s N
o C
1, C
2 Th
3, T
h4
No
Yes
Yes
No
20
29
M
Driv
er, R
TC
Mul
tiple
trau
mat
ic in
jurie
s Ye
s N
o Pe
lvis
fe
mur
N
o Ye
s Ye
s
25
36
M
Driv
er, R
TC
Mul
tiple
trau
mat
ic in
jurie
s N
o C
1, C
6-7
No
fem
ur
Yes
Yes
Yes
42
29
M
Driv
er, R
TC
Blee
ding
, inj
urie
s to
the
hear
t and
aor
ta
No
No
No
fem
ur, t
ibia
, fib
ula
No
Yes
Yes
47
23
F D
river
, RTC
Bl
eedi
ng, m
ultip
le tr
aum
atic
inju
ries
No
No
No
hum
erus
N
o Ye
s Ye
s 21
31
F
Driv
er, R
TC
Cer
ebra
l con
tusi
on/m
edul
la o
blon
gata
lesi
ons
Yes
C0-
1,C
2-3
No
tibia
, fib
ula
Yes
Yes
Yes
13
34
M
Driv
er, R
TC
Blee
ding
, mul
tiple
trau
mat
ic in
jurie
s N
o N
o Pe
lvis
hu
mer
us, f
emur
, tib
ia, f
ibul
a Ye
s Ye
s Ye
s
17
45
F D
river
, RTC
H
aem
orrh
agic
med
iast
inum
/rupt
ure
vena
cav
a N
o N
o N
o tib
ia, p
edis
N
o Ye
s Ye
s
19
35
M
Driv
er, R
TC
Suba
rach
noid
hae
mor
rhag
e/ce
rebr
al c
ontu
sion
N
o N
o N
o ul
na, r
adiu
s, fe
mur
, tib
ia, f
ibul
a Ye
s N
o Ye
s
22
20
M
Driv
er, R
TC
Pulm
onar
y co
ntus
ion
and
lace
ratio
n N
o N
o Th
9 N
o N
o Ye
s Ye
s
36
29
M
Driv
er, R
TC
Mul
tiple
trau
mat
ic in
jurie
s Ye
s N
o Th
5-6
hum
erus
, uln
a, ti
bia,
ped
is
Yes
Yes
Yes
46
37
M
Driv
er, R
TC
Mul
tiple
trau
mat
ic in
jurie
s Ye
s C
1-2
Pelv
is
No
Yes
Yes
Yes
53
31
M
Driv
er, R
TC
Mul
tiple
trau
mat
ic in
jurie
s Ye
s N
o Th
12, p
elvi
s N
o N
o Ye
s Ye
s
39
41
M
Driv
er, R
TC
Hae
mot
hora
x, a
ortic
rupt
ure
N
o N
o Pe
lvis
tib
ia
Yes
Yes
Yes
34
47
M
Driv
er, R
TC
Blee
ding
and
aor
tic la
cera
tions
N
o N
o Th
11, T
h12
No
No
Yes
No
28
38
M
Driv
er, R
TC
Blee
ding
and
mul
tiple
trau
mat
ic in
jurie
s Ye
s N
o N
o fe
mur
, cal
cane
us
Yes
Yes
Yes
19 c
ases
8
4 10
14
11
18
17
16
39
F Vi
tal a
ctiv
ity
Myo
card
ial i
nfar
ct
No
No
No
No
No
No
No
48
46
F H
ypot
herm
ia
Hyp
othe
rmia
and
into
xica
tion
(alc
ohol
) N
o N
o N
o N
o N
o N
o N
o
12
41
M
Vita
l act
ivity
M
yoca
rdia
l inf
arct
N
o N
o N
o N
o N
o N
o N
o
29
34
F Vi
tal a
ctiv
ity
Unk
now
n, in
toxi
catio
n (a
lcoh
ol)
No
No
No
No
No
No
No
43
33
M
Oth
er a
ctiv
ity
Blee
ding
due
to c
uttin
g in
jury
N
o N
o N
o N
o N
o N
o N
o
30
43
F Su
rger
y C
ardi
ac d
ysfu
nctio
n se
cond
ary
to s
urge
ry
No
No
No
No
No
No
No
38
49
M
Vita
l act
ivity
Ar
terio
scle
rotic
car
diac
dis
ease
N
o N
o N
o N
o N
o N
o N
o 18
37
M
Vi
tal a
ctiv
ity
Epile
ptic
sei
zure
/sub
arac
hnoi
d in
flam
mat
ion
No
No
No
No
No
No
No
45
35
M
Unk
now
n
Dia
betic
com
a N
o N
o N
o N
o N
o N
o N
o
51
23
M
Vita
l act
ivity
D
iabe
tic c
oma
No
No
No
No
No
No
No
15
32
M
Leis
ure
activ
ity
Unk
own
No
No
No
No
No
No
No
23
37
M
Oth
er a
ctiv
ity
Car
diac
dis
ease
N
o N
o N
o N
o N
o N
o N
o
31
31
M
Vita
l act
ivity
D
ehyd
ratio
n, p
erito
nitis
, par
alyt
ic s
mal
l bow
el
No
No
No
No
No
No
No
44
40
M
Oth
er a
ctiv
ity
Car
diac
dis
ease
N
o N
o N
o N
o N
o N
o N
o
52
48
M
Wor
king
Ar
terio
scle
rotic
car
diac
dis
ease
N
o N
o N
o N
o N
o N
o N
o
50
41
F Vi
tal a
ctiv
ity
Suba
rach
noid
hae
mor
rhag
e/ce
rebr
al a
neur
ysm
N
o N
o N
o N
o N
o N
o N
o
49
41
F Vi
tal a
ctiv
ity
Car
diac
dis
ease
N
o N
o N
o N
o N
o N
o N
o
40
27
F U
nkno
wn
Car
diac
dis
ease
, dia
bete
s m
ellit
us, i
ntox
icat
ion
No
No
No
No
No
No
No
54
22
M
Vita
l act
ivity
Ao
rtic
aneu
rysm
rupt
ure
and
card
iac
dise
ase
No
No
No
No
No
No
No
37
49
F Vi
tal a
ctiv
ity
Myo
card
ial i
nfar
ct
No
No
No
No
No
No
No
33
35
M
Vita
l act
ivity
Ar
terio
scle
rotic
car
diac
dis
ease
N
o N
o N
o N
o N
o N
o N
o 21
con
trols
0 0
0 0
0 0
0
Gen
der:
M (
mal
e), F
(fem
ale)
R
CT:
road
traf
fic c
rash
Vi
tal a
ctiv
ity: s
leep
, res
t
page 19
Table 2 Detailed description of the toxicological findings
Subject Age Gender Blood alcohol
concentration (‰) Drugs/ medicine
in blood/urine 26 21 M 2,08 No 24 22 F 0,00 No 35 33 M 0 No 14 20 M 0,88 No 20 29 M 0,10 Not tested 25 36 M 0,90 Metoprolol 42 29 M 0 Not tested 47 23 F 0 Not tested 21 31 F 0 No 13 34 M 0 Ketamine¥ 17 45 F 0 Not tested 19 35 M 1,89 Not tested 22 20 M 0 Valproate 36 29 M 0 Not tested 46 37 M 0 Not tested 53 31 M 0,22 Not tested 39 41 M (2,40)± Not tested 34 47 M 0 Citalopram 28 38 M 0 Not tested 19 cases 5 (BAC>0.5) 4
16 39 F 0 Not tested 48 46 F 1,82 No 12 41 M 0,78 Not tested 29 34 F 1,80 Cannabis¥ 43 33 M 0 Not tested
30 43 F 0 Clomipramine &
paracetamol† 38 49 M 0 Not tested 18 37 M 0 No 45 35 M 0 No 51 23 M 0 Not tested 15 32 M 0 No 23 37 M 0 Not tested 31 31 M 0 Not tested 44 40 M 0,28 Not tested 52 48 M 0 Not tested 50 41 F 0 Not tested 49 41 F 0 No 40 27 F 0 Cocaine¥ 54 22 M 0 No 37 49 F Not tested Not tested 33 35 M 0 No 21 controls 3 (BAC>0.5) 3
BAC: Blood alcohol concentration Gender: M (male), F (female) ± conc. in eyefluid (vitrous humor) † conc. of intoxication (overdose) ¥ narcotics/drugs
page 20
Tabl
e 3
Det
aile
d de
scrip
tion
of th
e m
icro
scop
ical
find
ings
on
the
10 μ
m s
ectio
ns
Subj
ect
Age
Gen
der
Frac
ture
of
a fa
cet
OC
F w
ith
bloo
d (0
-16
face
t)
OC
F w
ithou
t bl
ood
(0-1
6 fa
cet)
Blo
od in
any
jo
int s
pace
B
lood
in
any
fold
* B
lood
in
both
fold
s±
Ant
erio
r fol
d di
srup
ted
(0
-8 jo
ints
)
Post
erio
r fol
d di
srup
ted
(0
-8 jo
ints
)
Blo
od in
the
unde
rlyin
g bo
ne
26
21
M
No
0 10
N
o N
o N
o 3
7 Ye
s
24
22
F N
o 0
10
No
Yes
N
o 0
1 Ye
s
35
33
M
No
0 16
N
o N
o N
o 1
4 N
o
14
20
M
No
0 5
Yes
Yes
No
3 6
Yes
20
29
M
No
0 9
No
No
No
0 0
No
25
36
M
Yes
4 7
Yes
Yes
Yes
8 3
Yes
42
29
M
No
0 6
No
No
No
0 1
Yes
47
23
F N
o 0
10
Yes
Yes
Yes
3 5
Yes
21
31
F N
o 0
6 N
o Ye
s no
7
6 Ye
s
13
34
M
No
0 6
No
Yes
No
2 8
Yes
17
45
F N
o 0
8 N
o N
o N
o 0
2 Ye
s
19
35
M
No
0 9
Yes
No
No
1 4
Yes
22
20
M
Yes
1 13
Ye
s Ye
s Ye
s 8
7 Ye
s
36
29
M
No
0 10
Y
es
Yes
N
o 5
7 Ye
s
46
37
M
No
0 10
Y
es
Yes
N
o 3
2 N
o
53
31
M
Yes
0 13
N
o N
o N
o 3
7 N
o
39
41
M
Yes
1 15
Ye
s Ye
s Ye
s 6
5 Ye
s
34
47
M
No
0 10
Ye
s Ye
s Ye
s 1
3 Ye
s
28
38
M
No
0 8
No
No
No
2 5
Yes
19 c
ases
4
(p<0
.05)
6
(p<0
.01)
18
1 (5
9.2%
) (n
.s.)
9 (p
<0.0
1)
11
(n.s
.) 5
(p<0
.05)
56
(37.
3%‡ )
(p<0
.01)
83
(55.
3%‡ )
(p<0
.01)
15
(n
.s.)
16
39
F N
o 0
8 N
o N
o N
o 2
1 Ye
s
48
46
F N
o 0
9 N
o Ye
s N
o 2
0 Ye
s
12
41
M
No
0 13
N
o N
o N
o 0
3 N
o
29
34
F N
o 0
3 N
o N
o N
o 0
0 Ye
s
43
33
M
No
0 11
N
o N
o N
o 0
2 Ye
s
30
43
F N
o 0
8 N
o N
o N
o 0
3 N
o
38
49
M
No
0 13
N
o N
o N
o 0
1 Ye
s
18
37
M
No
0 10
N
o N
o N
o 0
0 Ye
s
45
35
M
No
0 13
N
o N
o N
o 1
6 Ye
s
51
23
M
No
0 13
N
o N
o N
o 2
6 Ye
s
15
32
M
No
0 10
N
o Ye
s N
o 0
2 Ye
s
23
37
M
No
0 9
No
No
No
1 7
Yes
31
31
M
No
0 11
N
o N
o N
o 1
0 Ye
s
44
40
M
No
0 7
No
Yes
No
2 2
No
52
48
M
No
0 7
No
No
No
0 1
Yes
50
41
F N
o 0
8 N
o Ye
s N
o 8
0 Ye
s
49
41
F N
o 0
7 N
o Ye
s N
o 1
6 Ye
s
40
27
F N
o 0
5 N
o Ye
s N
o 1
0 Ye
s
54
22
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page 21
Histomorphology of the lower cervical spine facet joints
Lars Uhrenholt1,2,3, Ellen Hauge3,4, Annie Vesterby Charles1,3, Markil Gregersen1
1 Institute of Forensic Medicine, University of Aarhus, Denmark
2 Nordic Institute of Chiropractic and Clinical Biomechanics, Part of Clinical Locomotion Science, Odense,
Denmark
3 Research Unit of Rheumatology and Bone Biology, Aarhus University Hospital, Aarhus Sygehus (NBG),
Denmark
4 Department of Rheumatology, Aarhus University Hospital, Aarhus Sygehus (NBG), Denmark
Corresponding author:
Lars Uhrenholt, Institute of Forensic Medicine, University of Aarhus
Brendstrupgaardsvej 100, 8200 Aarhus N, Denmark
E-mail: lu@forensic.au.dk, facsimile: 45-86125995, phone: 45-89429800
PAPER III
page 2
Abstract
Objectives
The purpose of this study was to examine anatomical variables of the lower cervical spine facet joints with
regard to age, gender, and exposure to trauma.
Methods
The lower four cervical spine motion segments (C4-C7 included) were obtained from forty subjects during
autopsy, twelve females (median age 40 years, range 22–49) and 28 males (median age 34.5 years, range
20–49 years). Ten μm thick histological sections were produced from 3-mm thick parasaggital slices going
through the facet joints bilaterally and evaluated with microscopy at random locations. Inter- and
intraobserver agreement was tested on four randomly selected facets from each subject.
Results
Significant age-, gender and trauma related changes in the cartilage and soft tissues were observed.
Females were less affected by changes in the cartilage than males. Anterior ad posterior synovial folds were
present in all but one joint. Moderate interobserver and good intraobserver agreement were achieved.
Conclusions
This study provides knowledge of the anatomy of the cervical spine facet joints. The findings support the
existing knowledge that males are more commonly affected by degenerative changes than females and that
these are common from young age. Histomorphometry confirms the presence of synovial folds throughout
the facet joints. Following spinal trauma pathological lesions may be produced in the facet joints and/or
accentuate already existing pathology. This study provides knowledge of the anatomy of the cervical spine
facet joints that may have relevance for patients with neck pain.
Keywords
cervical spine, facet joint, zygapophysial joint, histology, histomorphometry, autopsy, osteoarthritis, age,
gender
page 3
Introduction
The clinical relevance of age-related changes and osteoarthritis (OA) in the cervical spine facet joints is not
completely understood and the exact relation to neck pain is unknown, beyond the general fact that
increasing severity of OA is related to stiffness, decreased mobility and pain (1). The prevalence of early
degenerative changes such as superficial flaking (fibrillation) and fissuring of the articular hyaline cartilage,
vascular invasion of the tidemark and sclerosis of the subchondral bone plate is not known for the cervical
spine facet joints (1-3). Although numerous studies have investigated the cervical spine morphology
including the properties of the articular facets and related soft tissues (4-9) only limited knowledge is
available concerning studies of age-related cartilage and subchondral bony changes of human subjects (6).
The synovial folds (fat pads, meniscoids and inclusions) of the anterior and posterior margins of the lower
cervical spine facet joints have been described inconsistently in anatomical studies (4;10-16) and the joint
capsules of the cervical spine facet joints have been described in some detail (15). Histomorphometrical
studies have described the cervical spine anatomy, however in comparison to larger joints only limited
quantitative data currently exist regarding the properties of the cartilage, calcified cartilage and subchondral
bone of the cervical spine articular facets. (17-24). The general microscopical appearance of human synovial
joints, including the cervical spine facet joints, has been described in some detail (4-7) and general
histological classification systems are available for the description of these joints (2;6;16;25-28). However,
no validated system for microscopical grading of age-related changes in the cervical spine facet joints is
available, although a recent system originally developed for the lumbar spine facet joints has been utilised in
a preliminary evaluation of the upper cervical spine facets (16;27). Neck pain is an extremely common
symptom with high prevalence rates in Scandinavian countries compared to the rest of Europe and Asia
(29). Chronic neck pain following relatively minor trauma, e.g. low speed rear-impact collisions, is particularly
common and the lower cervical spine facet joints have been identified as a potential source of pain (30-32),
and nociceptive fibers have been identified in these structures (33;34). These findings have been supported
by nerve bloc and radio frequency neurotomy studies providing relief of symptoms after ablation of the
segmental nerve supply to the facet joints (35-37).
The purpose of this study was to describe the histomorphology of the lower cervical spine facet joints using
quantitative histomorphometric methods and to compare finding to age, gender and trauma.
page 4
Materials and methods
Materials
The lower cervical spines were obtained from forty subjects, twelve females (median age 40 years, range
22–49) and 28 males (median age 34.5 years, range 20–49 years). Nineteen died in a passenger car crash
and 21 died due to non-traumatic causes. Each specimen consisted of the cervical spine segments C4 to C7
including the facet joints bilaterally from C4-C5 to C7-Th1. In 39 subjects there were eight facet joints
available from each subject and in the remaining one subject there were only six facet joints available for
evaluation due to a bloc vertebrae at the C6-C7 level. Hence, the total number of facet joints available for
evaluation was 318, with 636 unique facets. The study was approved by the Scientific Ethics Committee,
Central Denmark Region.
Laboratory methods
The methods have previously been described (38). Each specimen was fixated in 70% ethanol followed by
hemisection along the midline saggital plane and embedded in methylmethacrylate (MMA) from where 3-mm
thick parasaggital slices were produced. All slices containing facet joint structures were re-embedded in
MMA and heavy-duty microtomal sections of 10 μm thickness were produced from each final bloc. These
histological sections were mounted on glass and stained un-deplastified with Masson Goldner-Trichrome
and examined with light microscopy using a BX51 Olympus© microscope.
Microscopical evaluation
A total of 1830 unique observations (approximately 46 observations per subject) were made, each with
reference to morphological variables including cartilage flaking (fibrillation), cartilage fissures, cartilage split,
vascular invasion, osteophytes, presence of the anterior and posterior folds and the integrity of these folds
(Table 1). Furthermore, included were observations obtained by measurements of projected images from a
BH2 Olympus© microscope with objectives x1 or x4, through a projection arm to a measuring table with a
final magnification factor on the table of 19.25 or 77.00 respectively (Table 1). This included the cartilage
length, the degree of overlap of the anterior and posterior folds in relation to the hyaline cartilage covering of
the facet, the thickness of the hyaline cartilage, the calcified cartilage and the subchondral bone (Figure 1).
The thicknesses were recorded of the facets from each histological section at one to five randomly chosen
points depending on the anterior to posterior length of the facet surface. The total articular cartilage
page 5
thickness was calculated as the sum of the calcified and hyaline cartilage thickness. All microscopical
evaluations were performed blinded with regard to the characteristics of the subjects (i.e. age, gender,
exposure to trauma, side, segment and level of the facet). For the purpose of inter- and intraobserver
agreement testing the morphological variables of four randomly chosen facets from each subject were
evaluated independently by two examiners who were blinded with regard to the characteristics of the
subjects. Hence, a total of 160 facets were eligible for this evaluation, however only 159 unique facets were
evaluated as the remaining one facet did not contain articular structures.
Statistical methods
The data were analysed with a linear regression model assuming linear association, normal distribution and
independence (homoskedasticity) of residuals. The regression model used for the morphological data
examined for correlation between gender, age and trauma versus no trauma and a reference person was
defined as a 35 years old male who had been killed in a road traffic crash (Table 2). The regression model
used for the histomorphometric data examined for correlation between gender, age, trauma versus no
trauma, side and facet per segment and a reference person (level) was defined as the left C4 inferior facet of
a 35 years old male who had been killed in a road traffic crash (Table 3). The potential effect of interaction
was not tested due to the limited number of subjects (n=40). The morphological variables were analysed for
inter- and intraobserver agreement using kappa statistics (39). The significance level was p < 0.05. Results
including 95 % confidence intervals were presented in square brackets, e.g. 75 μm [69-80]. All statistical
analyses were performed using Stata© 9 (StataCorp LP, College Station, USA).
page 6
Results
Descriptive morphology
Significant correlations to gender were predicted with females having 18 % [7–29] fewer facets with flaking
(p<0.01), 18 % [9–27] fewer facets with split (p<0.001), 13 % [1-26] fewer fissures overall (p<0.05) and 8 %
[1-15] fewer moderate fissures (p<0.05) than the male reference person (Figure 2) (Table 2). Significant
correlations to age were predicted with each decade contributing with an increase of 13 % [7–20] of facets
with flaking (p<0.001), 8 % [3-13] of facets with split (p<0.01) and 2 % [1-4] of facets with osteophytes
(p<0.01), and a decrease in the number of facets with a disrupted posterior fold by 10 % [3-18] (p<0.05). The
presence of split was significantly correlated to trauma with 10 % [1-18] more facets with split in the
traumatised group (p<0.05). Similarly, the presence of disrupted anterior and/or posterior folds was
associated with trauma, with 11 % [1-21] and 15 % [2-27] more folds being disrupted anteriorly and
posteriorly in the subject killed in a road traffic crash (p<0.05). No significant correlations were found for
vascular invasion, mild fissures and severe fissures with regard to any of the independent variables. The
presence of fissures did not correlate significantly with age.
Presence of the anterior and posterior folds
Intra-articular synovial folds were identified in all subjects (n=40), with anterior folds present in 100%
(318/318 anterior folds) and posterior folds present in 99.7% (317/318 posterior folds) of the respective folds
(Figure 3). In the remaining one joint (1/318) without identification of a posterior fold no evaluation could be
performed due to poor quality of the histological section.
Histomorphometry
Only the maximum cartilage length showed significant correlation to gender with a predicted 1.33 mm [0.46-
2.19] shorter cartilage in the female subjects (p<0.01) (Figure 4) (Table 3). There was a significant
correlation between age and an increase in the subchondral bone thickness of 0.04 mm [0.01-0.06] per
decade (p<0.01) approximately equivalent to an increase of 10% in comparison to the original thickness.
Significant systematic variations were generally observed between the cervical spine segments (i.e. C4-Th1)
(Figure 4 & 5). No statistically significant correlations were observed between; the thickness of the hyaline
cartilage, the calcified cartilage, the calcified cartilage percentage of the total cartilage, the anterior and
posterior fold overlap versus gender or age (Table 3). In none of these parameters were a significant
page 7
differences present between subjects exposed to trauma versus no trauma. The side was generally not
significant, except for minor differences in the subchondral bone thickness, maximum cartilage length and
anterior fold overlap.
Inter- and intraobserver agreement
The results from the inter- and intraobserver agreement evaluation are tabulated in detail in Table 4.
Regarding the interobserver agreement several variables had statistically significant kappa scores (p<0.001);
fissures (k=0.65), flaking (k=0.54), posterior fold disruption (k=0.51), split (k=0.31), and vascular invasion
(k=0.29). There were no statistically significant kappa scores for anterior fold disruption (k=0.09) and
osteophytes (k=-0.04), with (p=0.156) and (p=0.688) respectively. With regard to the intraobserver
agreement all variables had statistically significant kappa scores (p<0.001). The kappa scores were; fissures
(k=0.84), flaking (k=0.83), posterior fold disruption (k=0.74), split (k=0.79), vascular invasion (k=0.70),
anterior fold disruption (k=0.75), and osteophytes (k=0.65).
page 8
Discussion
This study of young individuals revealed significant relationship between age and flaking, split and
osteophytes. Age was significantly related to an increase in the subchondral bone thickness, however no
age-related differences were observed concerning the thickness of the hyaline and calcified cartilage.
Females had significantly fewer facets with flaking, splitting and fissures and the cartilage length was shorter
in comparison to males. The exposure to trauma was significantly correlated to cartilage split and disruption
of the folds. Flaking was the most common finding followed by split of the cartilage and the presence of
fissures of any severity. The mean overlap of the folds in relation to the underlying cartilage was almost
equal anteriorly and posteriorly with no significant differences with regard to gender or age.
Age-related changes
It is noteworthy that the age-range in this study was limited to 20-49 years which reduced the expected
alterations in age-dependent changes. Despite this we found, in accordance with previous studies,
significant correlation between age and several morphological variables (flaking, split and osteophytes) that
are all common in elderly subjects and related to OA (1;6;28). Similarly, the subchondral bone thickness was
correlating significantly with age, increasing approximately 10 % per decade which is in agreement with
previous observations (1;3;40). Other indicators of OA, such as osteophytes, duplication of the tidemark and
vascular invasion of the tidemark, were only present in limited numbers which is explained by the median
age (35 years) of the entire study population. Nonetheless, cartilage flaking, split and fissures were very
common in all ages in agreement with other studies (6;27). Fissures were common but did not reach
significant correlation with age although they are commonly encountered in OA and elderly subjects (1;28). It
was surprising to observe a significant decrease in the number of disrupted posterior folds with increasing
age and it can be speculated whether these observations occurred by chance or were consequences of
technical preparation of the histological sections.
Gender
The overall finding of significant correlation between gender and histological findings seen in OA (e.g.
cartilage flaking and splitting) is in agreement with other reports of males having a preponderance for
pathological facet joints (1;6). Similarly, the cartilage length was significantly shorter in females which has
also been reported previously (20;24).
page 9
Trauma
In a related study (unpublished observations) of the same material discrete fractures of the facets, bleeding
in the joints spaces and bleeding in the synovial folds were significantly related to the exposure to fatal road
traffic crash trauma. Disruption of both the anterior and posterior folds correlated significantly to trauma as
did cartilage split contributing to previous findings. The exact clinical relevance of these pathological findings
is uncertain. However, due to widespread individual biological variation in injury thresholds for these
variables it can be conjectures that some survivors from serious road traffic crashes may suffer similar
pathology and contribute to symptomatology (unpublished observations)(41). Furthermore, the lower cervical
spine facet joints have been found vulnerable to relatively minor acceleration forces which may cause
potentially injurious pathophysiological kinematics of these joints (42-44). As several post-mortem studies of
trauma victims have identified subtle lesions in the cervical spine facet joint capsules and synovial folds,
including disruption and bleeding, these structures are likely to have clinical importance in selected cases
(41;45).
Histology
The mean articular cartilage thickness of the cervical spine facet joint (C4 inferior process) in a reference
person was approximately 0.8 mm. The thickness varied depending on the spinal level indicating anatomical
differences in geometry reflective of developmental adaptations to different functional requirements. It was
interesting to observe that the calcified cartilage occupied approximately 10% percent of the complete
cartilage thickness which is somewhat higher than previous studies of other joints reporting values of
approximately 5% (3-8%) (3;40;46). The finding of synovial folds in all joints supports a number of previous
publications (4;14-16;47), although other studies have not been able to identify folds consistently (10;48).
Fletcher et al (48), examined 20 cadavers (two aged 10 and 19 years, and the remaining 18 subjects
between the age of 37-86 years) with photographic documentation of cryomicrotomal sections and
haematoxylin-eosin staining of decalcified sections and concluded that the menisci [folds] were nonexistent
at the age of 37 years and older. In the study by Yu et al (10), 10 decedents (mean age 48.3 years, range
10-69 years) were examined with photographic evaluation of cryomicrotomal sections and four types of
menisci [folds] were proposed despite the low number of subjects and the authors concluded that in the
lower cervical spine of adults, no menisci [folds] were present within the joint and the articular surfaces. In
contrast we found anterior and posterior synovial folds in all joints (except one), irrespective of age and
page 10
gender. The mean overlap of the anterior folds (16.1%) and posterior folds (16.9%) expressed as a
percentage of the underlying cartilage illustrates the overall overlap. However, in several parasaggital
sections of the facets we observed that the synovial fold covered the articular surface completely which
indicates that the fold have a heterogenous covering of the articular surface that is continuous over some
larger areas (Figure 6). It can be speculated that synovial folds in the cervical spine facet joints have a
protective and lubricative function as that of menisci (15;49).
Hyaline cartilage was found to cover the opposing joint surfaces in the majority of the joints. Occasionally, a
transitional zone was observed at the borders of the cartilage covering of the facets in which a gradual
replacement of the hyaline cartilage by fibrous cartilage took place. Hence, only rarely were free bony edges
encountered with periosteal covering, previously described as “cartilage gaps”(5). The discrepancies
between these findings may be explained by the different populations examined, where the previous study
only included six elderly subjects in contrast to 40 subjects in the age 20-29 years, and the orientation of
sectioning (although both methods used parasaggital orientation). Furthermore, we believe that detailed
morphology is best visualised by microscopy. Hence, in our study we find no support for the reported
findings of cartilage gaps and consequently no support of the pathomechanical theory of bony impact during
trauma as a cause of persistent neck pain.
Methodology
The overall interobserver agreement was moderate and was probably influenced by improperly defined
variables as well as different levels of experience between the observers. The overall intraobserver
agreement was good, and for all variables better than the interobserver agreement. This study used a similar
direction of sectioning (i.e. parasaggital) as related studies increasing the comparability (5;16;48;50-54).
However, despite randomisation of the locations of measurements the effect of orientation is unclear.
Preferably, a stereological unbiased evaluation using random sampling and orientation should be used in
order to examine a larger population with a wider age-range for the extent of age-related changes. The
potential effect of tissue shrinkage was not evaluated in this study. The method used in this study did not
allow evaluation of the overall severity of the morphological variables as only the worst case finding was
recorded for each observation. Ideally, the overall severity should be evaluated by considering the extent of
tissue affected (28).
page 11
Grading and staging of age-related and OA changes in the cervical spine facet joints may be performed with
the method of Pritzker et al (28). An alternative scoring system for cervical spine facet joint OA has been
published (16). However, as the weighted contributions from the variables were accumulated potential
differences in pathological severity between individuals were reduced. Hence, an adjusted classification
system based on the Pritzker et al (28) model targeting the cervical spine facet joints specifically, similar to
the methods used in this study, seems to be the most ideal solution.
Conclusion
Degenerative changes occur early in life in the lower cervical spine facet joints in both the cartilage and
subchondral bone, and have significant correlation to age. Males are more frequently and severely affected
by degenerative changes in the facet joints than females. Synovial folds are consistently found anteriorly and
posteriorly in the facet joints suggesting a yet unproven biological function. Spinal trauma produces
microscopical injuries to the soft tissues and cartilage in the facet joints, and may accentuate already existing
degenerative changes. It can be speculated that similar injuries may cause pain in survivors after road traffic
crashes.
page 12
Acknowledgements
The authors would like to acknowledge the original contributions from Professor DMSc. Flemming Melsen†,
the professional cooperation of the staff at the Institute of Forensic Medicine, University of Aarhus and the
Knoglelaboratoriet, Aarhus University Hospital. The strenuous and time-consuming efforts of Rita Ullerup in
careful preparation of the histological sections and the statistical counselling from Morten Frydenberg are
greatly appreciated. The study received support from the European Chiropractors Union Research Fund
Grant no. A.03-5, Switzerland, the Foundation for the Advancement of Chiropractic Research, Denmark and
the University of Aarhus Research Foundation, Denmark.
page 13
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Tidemark changes in osteoarthrosis--a histological and histomorphometric study in non-decalcified
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page 17
(47) Friedrich KM, Trattnig S, Millington SA, Friedrich M, Groschmidt K, Pretterklieber ML. High-field
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page 18
Figure 1 Schematic overview of the histomorphometric measurements
The cartilage length (d), and the anterior and posterior folds overlap of the underlying cartilage is
measured (d & e)(A). Each facet is measured at one to five randomly selected vertical lines through the
cartilage and underlying bone with regard to the thickness of the hyaline cartilage, the calcified cartilage
and the subchondral bone (B). The parallel lines resemble the 3-mm thick anatomical slices from where
each facet is measured and the numbers one to five correspond to the vertical lines in the figure above
(C).
page 19
Figure 2 The morphological variables
Vertical fissures are present in the deep and middle part of the cartilage, original magnification x4 (A).
Widespread superficial flaking/fibrillation of the cartilage, original magnification x10 (B). Large horizontal
split through the middle part of the hyaline cartilage, original magnification x4 (C). Example of vascular
invasion of the tidemark, original magnification x10 (D). All stained with Masson-Goldner trichrome.
page 20
Figure 3 Synovial folds of the cervical spine facet joints
A close-up view of the anterior synovial fold (F) which consist of fatty adipose tissue and strands of
fibrous tissue extending into the joint cavity, original magnification x4, Masson-Goldner trichrome
staining.
page 21
Figure 4 Mean maximum cartilage length
The mean values of the maximum cartilage length with 95 % confidence intervals as a function of
cervical spine segment and gender. Females have significantly shorter cartilage lengths than males and
these differ significantly between the cervical spine segments.
page 22
Figure 5 Mean articular cartilage thickness
The mean values of the mean thickness of the articular cartilage with 95 % confidence intervals as a
function of cervical spine segment and gender. There is no significant difference in thickness in relation
to gender or age, however the articular cartilage is significantly different between the spinal segments
being thinner in the lower cervical spine.
page 23
Figure 6 Heterogenous covering of the articular surface by the synovial folds
In this parasaggital section through the lateral part of a cervical spine facet joint there is complete
covering of the articular surfaces with a synovial fold, with the posterior fold (A) and anterior fold (B)
illustrated in close-up, original magnification x1 and x4, Masson-Goldner trichrome.
page 24
Table 1
Description of the anatomical variables
Definition Comments Morphological variables Flaking
Is there any tangential flaking or fibrillation of the surface of the hyaline articular surface?
Fibrillation/flaking anywhere of the cartilage surface
Split
Are there one or more horizontal splits of the hyaline cartilage?
Eyeballed percentage (a split is a matrix separation horizontal (0-60o to the articular surface)
Fissure
Are there one or more vertical fissures of the hyaline cartilage and what percentage does the worst represent of the total non-calcified hyaline cartilage thickness?
Eyeballed percentage (a fissure is a matrix separation vertical (60-90o to the articular surface). The fissures were grouped depending on whether the fissure affected none, < 50 % (mild), 50 – 99 % (moderate) or 100% (severe) of the cartilage
Vascular invasion Is there vascular invasion extending into the hyaline cartilage through the tidemark?
A blood vessel with or without cells resembling erythrocytes must be present extending into the hyaline cartilage
Osteophytes Are there any osteophytes developing at the joint margins?
Defined as new bone formation in the periphery of the joint margin – “an added outgrowth”
Anterior fold Is an anterior fold present and intact? Is tissue present that exhibits the structure and location of an anterior synovial fold and is it intact?
Posterior fold Is a posterior fold present and intact? Is tissue present that exhibits the structure and location of a posterior synovial fold and is it intact?
Histomorphometrical variables Cartilage length Length of the articular cartilage
Defined as the direct line between the anterior and posterior eyeballed borders of cartilage covered facets. Measured on the projected image and converted by a factor 1:19.25
Anterior fold overlap The degree of overlap of the facet in question by the anterior synovial fold
Defined as the part of the anterior fold extending into the joint centre from the line perpendicular to the cartilage length line at the anterior border. Measured on the projected image and converted by a factor 1:77
Posterior fold overlap The degree of overlap of the facet in question by the posterior synovial fold
Defined as the part of the posterior fold extending into the joint centre from the line perpendicular to the cartilage length line at the posterior border. Measured on the projected image and converted by a factor 1:77
Joint to tidemark (hyaline cartilage)*
Distance from joint space surface to the tidemark
Measured as the length along the perpendicular line to the articular cartilage surface on the projected image and converted by a factor 1:77
Tidemark to osteochondral junction (calcified cartilage)*
Distance from the tidemark to the osteochondral junction
Measured as the length along the perpendicular line to the articular cartilage surface on the projected image and converted by a factor 1:77
Osteochondral junction to subchondral bone edge*
Distance from the osteochondral junction to the first free space with bone marrow
Measured as the length along the perpendicular line to the articular cartilage surface on the projected image and converted by a factor 1:77
* each variable is measured at 1-5 sites on each 10 μm section
page 25
Estim
ate
95%
CI
Estim
ate
95%
CI
p-va
lue
Estim
ate
95%
CI
p-va
lue
Estim
ate
95%
CI
p-va
lue
Flak
ing
(%)
75[6
7-83
]-1
8[-2
9-(-7
)]<0
.01
13[7
-20]
<0.0
01-4
[-15-
(7)]
0.46
0S
plit
(%)
72[6
5-78
]-1
8[-2
7-(-9
)]<0
.001
8[3
-13]
<0.0
1-1
0[-1
8-(-1
)]<0
.05
Any
fiss
ure
(%)
58[4
9-67
]-1
3[-2
6-(-1
)]<0
.05
0[-7
-7]
0.98
5-2
[-14-
10]
0.73
10%
< fi
ssur
e <
50%
(%)
37[3
1-43
]-4
[-13-
4]0.
304
-5[-1
0-0]
0.05
93
[-6-1
1]0.
527
50%
= fi
ssur
e <
100%
(%)
18[1
3-23
]-8
[-15-
(-1)]
<0.0
54
[0-8
]0.
051
-4[-1
1-3]
0.23
2C
ompl
ete
fissu
re =
100
% (%
)3
[1-4
]-1
[-3-1
]0.
354
1[-1
-2]
0.32
9-1
[-2-1
]0.
562
Vas
cula
r inv
asio
n (%
)15
[9-2
0]-5
[-13-
3]0.
181
-4[-8
-1]
0.09
51
[-6-9
]0.
701
Ost
eoph
ytes
(%)
4[2
-6]
-1[-4
-1]
0.30
72
[1-4
]<0
.01
-1[-3
-1]
0.43
3A
nter
ior f
old
disr
uptio
n (%
)16
[8-2
3]2
[-8-1
3]0.
655
-1[-7
-6]
0.87
9-1
1[-2
1-(-1
)]<0
.05
Pos
terio
r fol
d di
srup
tion
(%)
33[2
3-43
]-8
[-22-
5]0.
210
-10
[-18-
(-3)]
<0.0
5-1
5[-2
7-(-2
)]<0
.05
Ref
eren
ce p
erso
n: 3
5 ye
ars
old
mal
e ki
lled
in a
road
traf
fic c
rash
Ref
eren
ce p
erso
n
Varia
ble
Exam
ple:
a 3
5 ye
ars
old
fem
ale
is p
redi
cted
to h
ave
flaki
ng in
app
roxi
mat
ely
57%
, i.e
. 18%
few
er fa
cets
than
mal
es (P
<0.0
1). T
here
is a
n ag
e-re
late
d in
crea
se in
the
num
ber o
f fac
et w
ith fl
akin
g eq
uiva
lent
to
13%
per
dec
ade
(p<0
.001
) and
no
sign
ifica
nt c
orre
latio
n w
ith tr
aum
a (p
=0.4
60)
Des
crip
tion
of th
e m
orph
olog
ical
find
ings
Tabl
e 2
Incr
ease
per
10
year
s
AGE
Con
trol v
s. C
ase
CAS
E/C
ON
TRO
LG
END
ER
Fem
ales
vs.
Mal
es
Estim
ate
95%
CI
Estim
ate
95%
CI
p-va
lue
Estim
ate
95%
CI
p-va
lue
Estim
ate
95%
CI
p-va
lue
Hya
line
carti
lage
thic
knes
s (m
m)
0.72
[0.6
7-0.
77]
-0.0
5[-0
.11-
0.02
]0.
152
0.00
[-0.0
4-0.
04]
0.96
60.
04[-0
.02-
0.10
]0.
180
Cal
cifie
d ca
rtila
ge th
ickn
ess
(μm
)79
[68-
90]
5[-8
-17]
0.47
17
[-1-1
4]0.
080
0[-1
2-12
]0.
972
Sub
chon
dral
bon
e th
ickn
ess
(mm
)0.
35[0
.31-
0.39
]0.
03[-0
.02-
0.07
]0.
229
0.04
[0.0
1-0.
06]
<0.0
10.
00[-0
.04-
0.04
]0.
852
Thic
knes
s of
the
tota
l arti
cula
r car
tilag
e (m
m)
0.80
[0.7
5-0.
85]
-0.0
4[-0
.10-
0.02
]0.
207
0.01
[-0.0
3-0.
04]
0.70
80.
04[-0
.02-
0.10
]0.
184
Max
imum
car
tilag
e le
ngth
(mm
)11
.35
[10.
66-1
2.04
]-1
.33
[-2.1
9-(-0
.46)
]<0
.01
-0.2
0[-0
.70-
0.30
]0.
435
0.54
[-0.2
9-1.
37]
0.20
4C
alci
fied
carti
lage
of t
otal
arti
cula
r car
tilag
e th
ickn
ess
(%)
10[9
-12]
1[-1
-3]
0.17
71
[0-2
]0.
123
-1[-2
-1]
0.48
9A
nter
ior f
old
over
lap
(%)
16[1
1-21
]0
[-6-6
]0.
974
1[-2
-4]
0.62
25
[0-1
1]0.
055
Pos
terio
r fol
d ov
erla
p (%
)17
[13-
21]
2[-2
-7]
0.31
41
[-2-4
]0.
460
3[-2
-7]
0.24
5
Ref
eren
ce le
vel:
the
C4
infe
rior f
acet
of a
35
year
s ol
d m
ale
kille
d in
a ro
ad tr
affic
cra
sh
Des
crip
tion
of th
e hi
stom
orph
omet
ric fi
ndin
gs
Tabl
e 3
Incr
ease
per
10
year
s
AGE
Con
trol v
s. C
ase
CAS
E/C
ON
TRO
LG
END
ER
Fem
ales
vs.
Mal
esR
efer
ence
leve
l
Varia
ble
Exam
ple:
a 3
5 ye
ars
old
fem
ale
has
a hy
alin
e ca
rtila
ge th
ickn
ess
equi
vale
nt to
that
of m
ales
(0.0
5 m
m th
inne
r, p=
0.15
2). T
here
are
no
age-
rela
ted
diffe
renc
es w
ith re
gard
to th
e th
ickn
ess
(p=0
.966
) and
ther
e is
no
sign
ifica
nt c
orre
latio
n w
ith e
xpos
ure
to
traum
a (p
=0.1
80).
page 26
Table 4
Inter- and intraobserver agreement of morphological variables
Simple agreement Kappa 95% CI p-value
Simple agreement Kappa 95% CI p-value
Variable
fissure* 89.1% 0.65 [0.53-0.76] < 0.001 95.4% 0.84 [0.72-0.95] < 0.001
flaking 79.7% 0.54 [0.37-0.71] < 0.001 91.8% 0.83 [0.67-0.98] < 0.001
posterior fold disruption 83.2% 0.51 [0.32-0.70] < 0.001 92.1% 0.74 [0.57-0.90] < 0.001
split 72.9% 0.31 [0.15-0.47] < 0.001 89.9% 0.79 [0.63-0.94] < 0.001
vascular invasion 82.1% 0.29 [0.13-0.45] < 0.001 93.0% 0.70 [0.55-0.86] < 0.001
anterior fold disruption 84.6% 0.09 [-0.08-0.26] 0.156 94.9% 0.75 [0.59-0.91] < 0.001
osteophytes 91.9% -0.04 [-0.21-0.13] 0.688 96.8% 0.65 [0.50-0.80] < 0.001
*: weighted kappa95% CI: 95% confidence interval
Interobserver agreement Intraobserver agreement
page 27
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