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MR imaging of degenerative disc disease
Accepted Manuscript Title: MR- Imaging of degenerative disc disease Authors: Nadja A. Farshad-Amacker MD Mazda Farshad MD, MPH Anna Winklehner MD Gustav Andreisek MD, MBA PII: DOI: Reference:
S0720-048X(15)00176-X http://dx.doi.org/doi:10.1016/j.ejrad.2015.04.002 EURR 7089
To appear in:
European Journal of Radiology
Received date: Revised date: Accepted date:
30-11-2014 2-4-2015 4-4-2015
Please cite this article as: Farshad-Amacker NA, Farshad M, Winklehner A, Andreisek G, MR- Imaging of degenerative disc disease, European Journal of Radiology (2015), http://dx.doi.org/10.1016/j.ejrad.2015.04.002 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
MR- Imaging of Degenerative Disc Disease
Nadja A. Farshad-Amacker, MD; 2Mazda Farshad, MD, MPH; 1Anna Winklehner,
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MD; 1Gustav Andreisek, MD, MBA
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Institute of Diagnostic and Interventional Radiology, University Hospital of Zurich, Zurich, Switzerland
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Department of Orthopaedic Surgery, Balgrist University Hospital, Zurich, Switzerland
Corresponding author:
Email: Tel./Fax:
Nadja A. Farshad-Amacker, MD. Department of Radiology, Raemistrasse 100, 8091 Zurich. Switzerland [email protected] +41 44255 34 86/ +41 4425544 43
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Abstract Magnet resonance imaging (MRI) is the most commonly used imaging modality for diagnosis of degenerative disc disease (DDD). Lack of precise observations and documentation of
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aspects within the complex entity of DDD might partially be the cause of poor correlation of radiographic finding to clinical symptoms. This literature review summarizes the current
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knowledge on MRI in DDD and outlines the diagnostic limitations. The review further
sensitizes the reader towards awareness of potentially untended aspects of DDD and the
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interaction of DDD and endplate changes. A summary of the available classifications for
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DDD is provided.
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DDD
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Keywords: spine; degeneration; disc; intervertebral disc; magnet resonance imaging; MRI;
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Introduction
Back pain is a widespread disorder with a life time prevalence of 70-85% 1. Degeneration of
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the intervertebral disc can cause back pain, but the presence of degenerative change seen radiographically does not necessarily correlate with the presence or severity of back pain as
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demonstrated by prospective study in asymptomatic volunteers without any history of
reported back pain or radiculopathy with however some form of degenerative change in more
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than 30% of the volunteers 2. However, Weishaupt et al 3 demonstrated that MRI changes,
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such as endplate abnormalities, if severe, can be helpful in prediction of a painful deranged disc. Although a direct association of lower back pain and DDD is not consistent, back pain is
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the typical symptom associated with DDD, mostly exacerbated by activities creating axial load or increased stresses in the intervertebral disc. DDD is further associated with other
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pathologies such as facet joint arthritis which is thought to be a result of increased load due to
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disc height collapse or segmental micro instability 4. The etiology of DDD is multifactorial and a number of potential etiological factors have been identified including genetics 5, gender , high mechanical stresses 6 such as heavy lifting 7, vascular insufficiency 8, smoking 9, and
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increased age 2, 6, 10. Further, hypolordosis has been demonstrated to be a potential etiological factor for accelerated DDD in a longitudinal study design 11. MRI has become the most commonly used imaging modality in the diagnosis of DDD. However, the correlation of MRI findings of DDD to clinical symptoms is not fully understood. This might be due to lack of precise observations and documentation of aspects within the complex entity of DDD. This review provides as an overview of the current knowledge regarding MR imaging in DDD, of the diagnostic limitations, and aims to sensitize the reader towards awareness of potentially untended aspects of DDD. A summary of the available classification for DDD is provided.
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MRI protocols of the spine MRI of the spine is generally performed with the patient in supine position. Upright MRI is feasible and favored by some groups due to the plausible explanation that axial loads on the
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intervertebral disc are reduced in supine position and that, as a consequence, dynamic events are ignored per definition with standard MRI. Currently, limited availability of upright MRI,
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its poor resolution, increased motion artifacts and associated high false-positive findings limit widespread use 12. However, a recent study has shown that about one third of patients with
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normal supine MRI had some form of DDD changes in upright MRI 13. Others have demonstrated that upright MRI can provide additional information when dynamic foraminal
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stenosis is suspected 14. Upright MRI with axial loading might be helpful in patients with
with positional pain differences 14.
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clinical symptoms that do not have a morphological correlate in supine MRI 13 or in those
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The standard MRI protocol for DDD typically includes two-dimensional (2D) sagittal T1-
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weighted (T1w) fast spin-echo (FSE), sagittal T2-weighted (T2w) FSE, and axial T2w FSE images. Most institutions add a short tau inversion recovery (STIR) sequence, a gradient echo
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sequence (particularly in the cervical spine) and coronal proton density-weighted (PDw), T2w or T1w sequence. The standard imaging protocols used at the institution of the primary and senior author is summarized in Table 1 and 2. Additional oblique sagittal images may aid in the evaluation of the cervical spine neural foramina, which as a result of their orientation can not be properly assess on standard sagittal images 15. High-resolution three-dimensional (3D) sequences with secondary reconstruction are particularly helpful in the cervical spine. Advantages are that secondary reformatted images can be better oriented along the oblique sagittal plane to show the foramen than standard 2D images and that the higher resolution allows better assessment of the relatively small cervical nerves roots. The latter is especially observed in axial images.
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The sagittal images are used to evaluate the vertebral bodies, intervertebral discs, the ligaments, facet joints, spinal canal and spinal cord and/or sac and intervertebral foramen. The STIR images are usually performed in the sagittal plane as well. Sites of active osteoarthritis
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may be detected on these images. They also provide information of the bone marrow as their fat suppression is usually very homogenous which eases detection of bone marrow changes.
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Axial images are useful for confirmation and evaluation of central canal stenosis, cord signal change, disc herniations, spinal cord compression, and nerve root compression. The facet
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joints are best assessed on axial images for the presence of arthrosis, synovitis and indirectly
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for segmental instability.
The coronal images, if performed, are particularly helpful for identification and classification
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of transitional vertebra, although the osseus bridging transitional vertebra can be identified on a single-slice midsagittal image as well 16. Coronal images also help to get an overview of the
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extent of scoliosis, if present and in detection of extraforaminal herniations.
Gradient echo sequences may be used to evaluate calcification of the ligaments, ossification
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of the posterior longitudinal ligament, and posterior endplate ridges, particularly in the cervical spine. Calcification in general implies as low signal intensity structure, although it can also imply as high signal intensity structure in T1w images, if containing lipids, melanin or bone marrow.
The use of contrast can be helpful in the postoperative setting. Some authors report superior evaluation of disc herniation postoperatively with pre- and early post-contrast images in order to be able to distinguish between epidural fibrosis and disc tissue 17. While there is a diffuse contrast-media uptake in epidural fibrosis/granulation tissue, there is only rim-enhancement in disc tissue 17. Further, partially healed chronic annular tears may demonstrate enhancement due to the presence of granulation tissue, not identified in normal T2w non-contrast MR images . 5
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MR neurography including diffusion tensor imaging (DTI) techniques for the spinal cord and nerve roots are currently only used for specific questions (e.g. in patients with
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neurofibromatosis) and for research, but not yet used in standard protocols 18.
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Intervertebral Disc
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Normal anatomy and imaging appearance
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The intervertebral disc consists of a centrally located nucleus pulposus encircled by the annulus fibrosus, which is attached to the cartilaginous endplates. The annulus fibrosis is a
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strong fibrocartilaginous structure with dense fibers, containing primarily type I collagen. In contrast, the nucleus pulposus is a very soft structure mainly containing water (70-90%) and
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proteoglycans in a loose network of Type II collagen 19. In adults (>30years) in the center of
fibrous plate 20.
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the disc a transversely oriented band of hypointense signal is often visible representing a
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The intervertebral discs of the cervical and thoracic spine are much thinner as compared to the intervertebral discs of the lumbar spine. Further, the annulus fibrosis is thicker in the lumbar spine than in the cervical or thoracic spine 2, 10, 21. The intervertebral disc is mainly avascular and supplied by passive diffusion from the vertebral endplates. In fact, the L4/5 disc space is the largest avascular structure in the body 22. The nucleus pulposus is hypointense compared to the vertebral bodies on T1w images and hyperintense on T2w images due to its high water and proteoglycan content. By contrast, the annulus fibrosus shows lower signal intensities on T1w and T2w images 21. The endplates are well defined and smooth with an intact covering of cortical bone. Age-related changes or agedependent degeneration of the intervertebral disc include mainly decreasing disc cellularity and alteration of the extracellular matrix 23. 6
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Pathologic appearance and features of DDD on MRI
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Dehydration and degeneration of the intervertebral disc Disc degeneration is characterized by presence of dehydration of the disc 24. Disc dehydration
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results from decreased proteoglycans that normally function to bind water. There is a relative
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increase of type I collagen within the nucleus pulposus of degenerated discs 25.
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The disc matrix turnover can be divided in three phases. Phase I is described as growth period (synthesis of aggrecan and procollagens I, II and increased denaturation of type II collagen)
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between 0-15 years of age; phase II (maturation and ageing phase) is characterized by reduction in synthesis (except for type I procollagen) along with reduction in denatured type
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II collagen; phase III (degeneration and fibrotic phase) by increased denatured type II
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collagen and increase in synthesis of type I procollagen (40-80 years) 26.
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On MRI, disc degeneration manifests as loss of intranuclear T2 hyperintensity and subsequent loss of disc height. Pfirrmann et al. classified disc degeneration based on a combination of (a) disc structure, (b) distinction between the nucleus pulposus and the annulus fibrosus; (c) signal intensity and (d) the intertervertebral disc height 27 (Figure 1). Griffith et al modified the Pfirrmann grading system adding three more stages that included a quantitative measurement of the disc height reduction in severe dehydrated discs 28. Newer MR techniques such as T2/T2*- mapping 29, T1-Rho 30, chemical exchange saturation transfer 31, delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) 32, Sodium MRI 33 and Spectroscopy 34 allow evaluation of disc degeneration based on chemical composition of the disc, mainly by evaluation of proteoglycan content. This might result in detection of disc degeneration at an earlier stage 33. However, those techniques are still under development and 7
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not yet included in clinical routine. The main reasons for that are low signal to noise ratios, unavailability on standard MRI scanners or long scanning times 35. Further, more studies are warranted to prove their superiority compared to the Pfirrmann scoring system. Particularly,
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taking into account that early MRI changes often reflects the normal physiologic process of
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aging 36.
Intra-discal gas might be difficult to identify on MRI. The usually impression is that of low
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signal intensity on both T1w and T2w images. When present, intra-discal gas may be seen in association with peripheral annular high signal intensity on T2w images 37. A characteristic
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can however not be appreciated on MR images.
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sign for intradiscal gas is its presence in extension and disappearance in flexion 37. The latter
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Anulus fibrosus tears
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Three forms of annular tears have been described: (a) concentric, (b) radial and (c) transverse tears, however to the knowledge of the authors differentiation of these three forms with the
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use of MRI is challenging. Annular tears have been found in asymptomatic adults, however the concentric tears seem to be more often found in normal discs as compared to transverse tears that are found in degenerative discs 22. Some suggest that annular tears occur early in the course of DDD and may lead to faster development of DDD 38. However a recently performed longitudinal study showed that an annular tear defined as a hyperintensity zone on T2w images within the annulus fibrosus does not accelerate disc degeneration when compared to matched control discs 39. Annular tears are in generally detected by high signal intensity on T2- weighted images (Figure 2). The use of gadolinium might increases the sensitivity for detecting annular tears due to enhancement of granulation tissue within a healing annular tear 40. However in some annular tears the T2w hyperintense signal remains over several years 39 and thus further 8
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studies are needed to evaluate when and which annular tears undergo healing with granulation tissue repair.
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Bulging/Protrusion/Extrusion of the disc In general disc herniation is a result of disc degeneration; herniation without degeneration is
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extrusion is best evaluated using sagittal and axial images.
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rarely seen and typically is caused by extensive traumatic forces. A disc protrusion or
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It is important to differentiate between a bulge and a herniation using axial images (Figure 3) . A bulging disc is often seen in asymptomatic individuals and possibly only a consequence
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of normal aging disc. It is further important to differentiate between a protrusion and an extrusion, particularly in case of neural compression. While an extruded disc could be
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surgically removed without need of an annulotomy, a protrusion or bulge needs an
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annulotomy. The distinction between a disc bulge and further between a protruded and extruded herniation is mandatory that surgeons know in advance whether annulotomy and
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nucleotomy is needed or not. Surgical time is increased with the need of an annulotomy and nucleotomy and subsequent faster disc degeneration may occur. The latter has been shown in animal models where DDD was induced by as the means of nucleotomy 42. A disc bulge is a circumferential prolapse of the intervertebral disc (at least >50% of the circumference of the disc) 41, 43 but the annulus fibrosus stays intact. A disc bulge is very often seen in asymptomatic individuals and mostly asymptomatic. A herniation is further differentiated into (a) protrusion, (b) extrusion and (c) sequestration (Figure 3) while a sequestration is correctly defined as a subgroup of an extrusion. Herniations are further described according to the location (central, paracentral, foraminal and extraforaminal) (Figure 4). Some authors prefer the term left or right central instead of paracentral 41. 9
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A protrusion is defined when the protruded disc material extends <50% of the disc circumference and if the size of the base/neck of the protruded material exceeds the maximal length of the protruded material 41, 43. A protrusion can further be classified in focal (<25% of
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the disc circumference) or broad-based (25-50% of the disc circumference) 41, 43. In a protruded disc, at least some fibers of the overlying annulus and posterior longitudinal
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ligament remain intact 37. Surgically, a protrusion might better be classified into the group of disc bulging, as it often needs annulotomy for removal.
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An extrusion is defined if the size of the base/neck of the protruded material is less than the
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maximal length of the protruded material 41, 43. With extrusions and sequestrations, the annulus fibrosus and sometimes the overlying posterior longitudinal ligaments are focally
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disrupted. A free disc fragment or sequestration is defined as a piece of disc that is separated from the original disc. The fragment may migrate superiorly or inferiorly with respect to the
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disc space and rarely may be located intradurally 37.
In addition to location (Figure 4), disc herniations should be described in relation to the nerve
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roots, with particular attention to the degree of nerve contact, displacement or compression 44. Foraminal nerve compression is best evaluated using sagittal T1w images in the lumbar and thoracic spine. A grading system for foraminal nerve compression was introduced by Wildermuth et al 45 (Grade 0: absence of foraminal stenosis; Grade 1:. mild foraminal stenosis (<50%); Grade 2: moderate foraminal stenosis (>50%); Grade 3: severe foraminal stenosis (nerve root collapse)). Nerve roots in the intervertebral foramen are located superior to the intervertebral discs in the lumbar spine. Therefore, a foraminal herniation doesn’t necessarily affect the nerve root. In the lumbar spine a clinically symptomatic nerve irritation/compression is most often cause of multifactorial process (disc herniation, dorsal spondylophtes, flavum ligament hypertrophy and arthrosis of the facets joint). Complete
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absent fat around the nerve root in the intervertebral foramen is consistent with nerve root compression in the lumbar spine. In contrast, in the cervical spine the nerve root at the intervertebral foramen is located at the
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same level or slightly below the intervertebral disc 46. Therefore, small protrusions might already cause symptoms and sagittal oblique or high-resolution 3D- images are of utmost
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importance for the detection of such small protrusions. Maintained fat around the nerve root in the intervertebral foramen is an unreliable sign in the cervical spine. This is also
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demonstrated in a newly introduced grading system for cervical spine foraminal stenosis, using oblique sagittal sequences. There, the authors anecdotally demonstrate the case of a
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patient with only a grade 1 foraminal stenosis suffering from radiculopathy 47.
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A grading system to grade the disc herniation in relation to a recessal nerve root irritation was proposed by Pfirrmann et al 44 for the lumbar spine: Grade 1 describes contact to the nerve
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root without displacement or compression; grade 2 refers to nerve root displacement by disc
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material; and grade 3 encompasses nerve root compression 44 (Figure 5). This grading system has been shown to be reliable with a good interreader agreement for the higher grades
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(comparing grades I- III), but was slightly less reliable in distinguishing normal roots versus grade I (contact) 44.
Indirect signs for nerve root compression are enlargement of the nerve root (pre- and post compression) and nerve root enhancement after gadolinium application. The underlying mechanism for nerve enlargement and enhancement may relate to inflammation and alteration of the blood/nerve barrier 48.
Bone marrow changes of the endplates Endplate changes on MRI were first described in the 1980s and classified into three types by Modic et al according to the underlying bone marrow signal change 49, 50.
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Modic type I changes are manifested as T1w hypointense and T2w hyperintense corresponding to a stress reaction of the bone marrow (Figure 6). Percutaneous biopsies demonstrated the underlying patho-morphological changes namely subchondral fractures and
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vascularized fibrous tissue replacing the hematopoetic bone marrow 49-51. Modic type II changes are seen if the bone marrow undergoes fatty replacement resulting in increased signal
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on T1w and intermediate to high signal on T2w (Figure 6). Modic type III changes are seen as T1 as hypointensities and T2 as hypointensities, reflecting the presence of dense woven
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bone 50 (Figure 6).
can even convert to normal bone marrow 51, 52.
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The progress of Modic changes is not necessarily orderly from I to III, Modic type I changes
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Modic changes seem to be a specific (97%), but insensitive (23%) for painful lumbar disc disease 53. Type I and III changes seem to be more often associated with low back pain (73%)
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than Type II changes (11%) 54.
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Future research focuses towards detection of endplate changes prior to bone marrow changes by direct evaluation of the cartilaginous endplates, e.g. with ultrashort echo time MR imaging or by perfusion evaluation of the endplate 56. Recently, it was reported that perfusion of
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endplates changes using dynamic contrast-enhanced MRI profiles was significantly different if degenerative marrow changes were visible 56.
Interaction of disc degeneration and endplate changes Some authors assume that the disc degeneration may result from initial endplate damage leading to decreased disc nutrition. Changes in diffusion with different degrees of degeneration based on the Pfirrmann classification seem to correlate to a newly introduced endplate damages score 57 (Figure 7). Pfirrmann grades seem also to correlate with the Modic changes 58. However, further studies are required to determine whether the endplate changes cause disc degeneration or vice versa. 12
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Most common levels of degenerative disc disease
Cervical spine
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Disc herniations and Modic changes in the cervical spine are most often observed at C5/6 and C6/7 (Figure 8a) and often reported in young patients (third to fourth age decade) 37. The loss
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of T2w signal hyperintensity of a normal intervertebral disc in T2w images is not as helpful as
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in the lumbar spine for identification of degeneration 37 because the intervertebral disc of the cervical spine is in general of lower signal intensity compared to the lumbar spine (Figure
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8a).
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Thoracic spine
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DDD in the thoracic spine is less common compared to the cervical or lumbar spine. Disc herniation is rare and is most often seen at the level Th11/12 and Th12/L1, most likely due to
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free ending or floating ribs 59 as a result of a lever arm effect of the rigid construct above. Above Th11, the ribs and the sternum serve as a stabilizing construct for the whole thoracic spine, comparable to a fusion 37 and Th1-Th10 vertebra seem therefore less prone to degeneration.
Lumbar spine
DDD of lumbar spine is most observed at the L4/5 and L5/S1 level (Figure 8b). This however does not apply to subjects with lumbosacral transitional vertebrae (LSTV), as the transitional level seems protected as compared to the level above the LSTV, which is prone to DDD 60. This observation has been observed particularly in higher type of LSTV according to the Castellvi Classification, where posterior osseous bridging limits segmental motion 60. 13
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Conclusion
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MRI is the most commonly used imaging modality in diagnosis of DDD. Standard MRI is performed in the supine position and cannot reflect dynamic aspects of DDD. Classifications/
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grading systems of DDD and associated pathologies such as endplate changes or affection of
neural structures are described and should be used in order to quantify DDD and differentiate
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the complex entity of DDD. The differentiation of disc bulging and herniation is of immediate
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clinical and surgical relevance while protrusion of the disc should better be classified as a form of disc buldging rather than disc herniation, as if surgically treated, former needs often
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surgical annulotomy.
Lack of precise observations and documentation of aspects within the complex entity of DDD
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might partially be the cause of poor correlation of radiographic finding to clinical symptoms.
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[38] Sharma A, Pilgram T, Wippold FJ. Association between annular tears and disk
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[39] Farshad-Amacker NA, Hughes AP, Aichmair A, Herzog RJ, Farshad M. Is an annular
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tear a predictor for accelerated disc degeneration? European spine journal : official publication of the European Spine Society, the European Spinal Deformity Society, and the European Section of the Cervical Spine Research Society 2014.
[40] Ross JS, Modic MT, Masaryk TJ. Tears of the anulus fibrosus: assessment with GdDTPA-enhanced MR imaging. AJR American journal of roentgenology 1990;154(1):159-62. [41] Fardon DF, Milette PC, Combined Task Forces of the North American Spine Society ASoSR, and American Society of Neuroradiology. Nomenclature and classification of lumbar disc pathology. Recommendations of the Combined task Forces of the
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North American Spine Society, American Society of Spine Radiology, and American Society of Neuroradiology. In. Spine, 2001: E93-E113 [42] Guder E, Hill S, Kandziora F, Schnake KJ. [Partial nucleotomy of the ovine disc as an
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[44] Pfirrmann CWA, Dora C, Schmid MR, Zanetti M, Hodler J, Boos N. MR image-based
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[45] Wildermuth S, Zanetti M, Duewell S, et al. Lumbar spine: quantitative and qualitative assessment of positional (upright flexion and extension) MR imaging
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[46] Demondion X, Lefebvre G, Fisch O, Vandenbussche L, Cepparo J, Balbi V. Radiographic anatomy of the intervertebral cervical and lumbar foramina
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[47] Park H-J, Kim SS, Lee S-Y, et al. A practical MRI grading system for cervical foraminal stenosis based on oblique sagittal images. In. Br J Radiol, 2013: 20120515
[48] Kobayashi S, Yoshizawa H, Yamada S. Pathology of lumbar nerve root compression. Part 1: Intraradicular inflammatory changes induced by mechanical compression. In. J Orthop Res, 2004: 170-9 [49] de Roos A, Kressel H, Spritzer C, Dalinka M. MR imaging of marrow changes adjacent to end plates in degenerative lumbar disk disease. In. AJR American journal of roentgenology, 1987: 531-4
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[50] Modic MT, Steinberg PM, Ross JS, Masaryk TJ, Carter JR. Degenerative disk disease: assessment of changes in vertebral body marrow with MR imaging. In. Radiology, 1988: 193-9
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[51] Vital JM, Gille O, Pointillart V, et al. Course of Modic 1 six months after lumbar posterior osteosynthesis. In. Spine, 2003: 715-20- discussion 21
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[52] Hutton MJ, Bayer J, Sawant M, Sharp DJ. VERTEBRAL ENDPLATE CHANGES: THE
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NATURAL HISTORY AS ASSESSED BY CONSECUTIVE MAGNETIC RESONANCE IMAGING. In. The Bone & Joint Journal, 2005: 233
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[53] Braithwaite I, White J, Saifuddin A, Renton P, Taylor BA. Vertebral end-plate (Modic) changes on lumbar spine MRI: correlation with pain reproduction at
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lumbar discography. In. European spine journal : official publication of the European Spine Society, the European Spinal Deformity Society, and the
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European Section of the Cervical Spine Research Society, 1998: 363-8
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[54] Toyone T, Takahashi K, Kitahara H, Yamagata M, Murakami M, Moriya H. Vertebral bone-marrow changes in degenerative lumbar disc disease. An MRI study of 74
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patients with low back pain. In. J Bone Joint Surg Br, 1994: 757-64
[55] Bae WC, Statum S, Zhang Z, et al. Morphology of the Cartilaginous Endplates in Human Intervertebral Disks with Ultrashort Echo Time MR Imaging. In. Radiology, 2013: 564-74
[56] Savvopoulou V, Maris TG, Koureas A, Gouliamos A, Moulopoulos LA. Degenerative endplate changes of the lumbosacral spine: dynamic contrast-enhanced MRI profiles related to age, sex, and spinal level. In. Journal of magnetic resonance imaging : JMRI, 2011: 382-9 [57] Rajasekaran S, Venkatadass K, Naresh Babu J, Ganesh K, Shetty AP. Pharmacological enhancement of disc diffusion and differentiation of healthy,
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ageing and degenerated discs : Results from in-vivo serial post-contrast MRI studies in 365 human lumbar discs. In. European spine journal : official publication of the European Spine Society, the European Spinal Deformity
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Society, and the European Section of the Cervical Spine Research Society, 2008: 626-43
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[58] Albert HB, Briggs AM, Kent P, Byrhagen A, Hansen C, Kjaergaard K. The prevalence
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of MRI-defined spinal pathoanatomies and their association with modic changes in individuals seeking care for low back pain. In. European spine journal : official
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publication of the European Spine Society, the European Spinal Deformity Society, and the European Section of the Cervical Spine Research Society, 2011:
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1355-62
[59] Blumenkopf B. Thoracic intervertebral disc herniations: diagnostic value of
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magnetic resonance imaging. In. Neurosurgery, 1988: 36-40
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[60] Farshad-Amacker NA, Herzog RJ, Hughes AP, Aichmair A, Farshad M. Associations between lumbosacral transitional anatomy types and degeneration at the
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transitional and adjacent segments. The spine journal : official journal of the North American Spine Society 2013.
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Legend to the figures
Figure 1. Examples of the different grades of lumbar disc degeneration according to
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Pfirrmann et al 27. Schematic and corresponding T2w sagittal MR images show (a) grade Ihomogenous, bright hyperintense disc structure and a normal disc height, (b) grade II-
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inhomogenous, but hyperintense disc structure with clear differentiation between nucleus and
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annulus and normal disc height, (c) grade III- inhomogenous, intermediately gray disc with an unclear distinction between nucleus and annulus, the disc height is normal or slightly
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decreased, (d) grade IV- inhomogenous, hypointense dark-gray disc with a lost distinction between nucleus and annulus and with the disc height normal or moderately decreased, (e)
annulus and a collapsed disc space.
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grade V- inhomogenous, hypointense black disc with lost distinction between nucleus and
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Note: Pfirrmann classification was described using T2w sagittal FS FSE sequences (TR/TE
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5000/130). Our lumbar spine protocol is performed with TR/TE: 5000/93 and note that not all
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of the here represented images were performed with FS.
Figure 2. Example of an annular tear. (a) Sagittal and (b) axial T2w FSE show a hyperintense disruption of the annulus paracentral on the right side (arrow). Note the recessal nerve root deviation on the same side (arrowhead)
Figure 3. Schematic illustration and the corresponding axial T2w FSE MR images of disc a) bulging (arrows), b) protrusion (arrows), c) extrusion (arrow) and d) sequester (arrow). The signal of the sequestered fragment changes slightly to hyperintense with progression and the
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fragment may migrates, in this case the fragment is located above the disc level, on the level of the next vertebral body. Note that the neck/base of an extruded disc is equal or smaller than the maximal length of the extruded disc material in contrast to a protrusion where the
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neck/base exceeds the maximal length of the protruded material.
Figure 4. (a) Schematic illustration of potential locations of a disc herniations in the axial
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plane. T2w FSE MR images of a (b) median/central disc extrusion (arrow), (c)
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paracentral/recessal broad based protrusion (arrow), (d) foraminal broad based protrusion
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(arrow) and (e) an extraforaminal disc herniation (arrow).
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Figure 5. Schematic Illustrations and corresponding axial T2w FSE MR images of different
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grades of nerve root compromise recessal due to disk herniation described by Pfirrmann et al , here slightly modified. a) a median to paracentral disc herniation (a broad-based protrusion
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on the MR-image) without contact to the nerve root (arrow). The epidural fat layer and cerebrospinal fluid between the nerve root and the herniation is preserved. b) Median to paracentral disc herniation (an extrusion on the MR-image) with contact to the nerve root, but without a relevant displacement (arrow). c) Paracentral disc herniation (a broad-base protrusion on the MR-image) with displacement of the recessal nerve root dorsally (arrow). d) Large paracentral disc herniation (an extrusion on the MR image) with recessal nerve root compression due to the disc herniation against the wall of the spinal canal (arrow).
Figure 6. Sagittal T1w and T2w MR images show the different types of Modic changes 50. Type I, represents bone marrow edema (T1w hypointense, T2w hyperintense); type II, 24
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represents fatty bone marrow replacement (T1w hyperintense, T2w hyperintense); type III,
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represents presence of dense woven bone (T1w hypointense, T2w hypointense).
Figure 7. Example of the severity of the endplate damage, scored according to Rajasekaran et
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al 57. Schematic and corresponding sagittal T1w FSE images show (a) type I- normal
endplate, with no interruption, (b) type II is a thinning of the endplate, no obvious break, (c)
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type III is a focal endplate defect with established disc marrow contact but with maintained
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endplate contour, (d) type IV is defined as endplate defects less than 25% of the endplate area (arrow), (e) type V is defined as endplate defects up to 50% of the endplate area (arrow and
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arrow head in (d)), (f) type VI is defined as extensive damaged endplates up to total
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destruction. Type IV-VI are often associated with Modic changes in the bone marrow.
Figure 8. T2w FSE MR images show typical locations for disc degeneration in the (a)
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cervical spine at the levels C5/6 and C6/7 (*) and in the lumbar spine at the levels L4/5 and L5/S1 (*).
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Tables Table 1. MR protocol lumbar spine on 1,5T scanner Sag T1w Sag T2w Sag STIR FSE FSE
Axial T2w FSE
Coronal T2w FSE
500
5000
3600
4000
4500
TE
9.5
95
35
101
101
3
3
3
123
32
18
22
NEX
1
1
1
FOV (mm)
280
280
280
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3
3
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Slice thickness (mm) ELT
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TR
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1
220
1
280
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307 x 384 336 x 448 288 x 320 336 x 448 288 x 384 Matrix Spacing 0.6 0.6 0.6 0.3 0.6 (mm) Sag, sagittal; T1w, T1-weighted; FSE, fast spin-echo; T2w, T2-weighted; STIR, short-tau inversion recovery; CM, contrast media TR, repetition time; TE, echo time; ETL, echo train length; NEX, number of excitations; FOV, Field of view.
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Table 2. MR protocol cervical spine on 1,5T scanner Sag T1w FSE
Sag T2w FSE
Sag STIR
Axial T2w Sag oblique FSE T2w FSE
3D GRE
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690 3500 4000 3500 3500 532 TR 9.5 126 39 91 131 15 TE 3 3 3 3 2.5 3 Slice thickness (mm) 135 30 18 10 26 ELT 2 1 3 3 1 3 NEX 220 220 220 160 220 160 FOV (mm) 269 x 384 307 x 512 269 x 384 240 x 320 269 x 448 256 x 256 Matrix 0.3 0.3 0.3 0.1 0.1 0.3 Spacing (mm) Sag, sagittal; T1w, T1-weighted; FSE, fast spin-echo; T2w, T2-weighted; STIR, short-tau
inversion recovery; CM, contrast media TR, repetition time; TE, echo time; ETL, echo train
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length; NEX, number of excitations; FOV, Field of view.
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Acknowledgments:
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The authors thank the University Hospital of Zurich for providing the MR images used in this article and the Swiss National Fond who supported individual funding of Nadja A. FarshadAmacker.
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Highlights
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1. This systematic literature review summarizes the current knowledge on MR imaging in degenerative disc disease. 2. Different classification systems for segmental spine degeneration are summarized. 3. It outlines the diagnostic limitations of MR imaging.
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S0720-048X(15)00176-X http://dx.doi.org/doi:10.1016/j.ejrad.2015.04.002 EURR 7089
To appear in:
European Journal of Radiology
Received date: Revised date: Accepted date:
30-11-2014 2-4-2015 4-4-2015
Please cite this article as: Farshad-Amacker NA, Farshad M, Winklehner A, Andreisek G, MR- Imaging of degenerative disc disease, European Journal of Radiology (2015), http://dx.doi.org/10.1016/j.ejrad.2015.04.002 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
MR- Imaging of Degenerative Disc Disease
Nadja A. Farshad-Amacker, MD; 2Mazda Farshad, MD, MPH; 1Anna Winklehner,
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MD; 1Gustav Andreisek, MD, MBA
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1
1
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Institute of Diagnostic and Interventional Radiology, University Hospital of Zurich, Zurich, Switzerland
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Department of Orthopaedic Surgery, Balgrist University Hospital, Zurich, Switzerland
Corresponding author:
Email: Tel./Fax:
Nadja A. Farshad-Amacker, MD. Department of Radiology, Raemistrasse 100, 8091 Zurich. Switzerland [email protected] +41 44255 34 86/ +41 4425544 43
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Abstract Magnet resonance imaging (MRI) is the most commonly used imaging modality for diagnosis of degenerative disc disease (DDD). Lack of precise observations and documentation of
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aspects within the complex entity of DDD might partially be the cause of poor correlation of radiographic finding to clinical symptoms. This literature review summarizes the current
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knowledge on MRI in DDD and outlines the diagnostic limitations. The review further
sensitizes the reader towards awareness of potentially untended aspects of DDD and the
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interaction of DDD and endplate changes. A summary of the available classifications for
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DDD is provided.
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DDD
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Keywords: spine; degeneration; disc; intervertebral disc; magnet resonance imaging; MRI;
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Introduction
Back pain is a widespread disorder with a life time prevalence of 70-85% 1. Degeneration of
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the intervertebral disc can cause back pain, but the presence of degenerative change seen radiographically does not necessarily correlate with the presence or severity of back pain as
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demonstrated by prospective study in asymptomatic volunteers without any history of
reported back pain or radiculopathy with however some form of degenerative change in more
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than 30% of the volunteers 2. However, Weishaupt et al 3 demonstrated that MRI changes,
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such as endplate abnormalities, if severe, can be helpful in prediction of a painful deranged disc. Although a direct association of lower back pain and DDD is not consistent, back pain is
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the typical symptom associated with DDD, mostly exacerbated by activities creating axial load or increased stresses in the intervertebral disc. DDD is further associated with other
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pathologies such as facet joint arthritis which is thought to be a result of increased load due to
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disc height collapse or segmental micro instability 4. The etiology of DDD is multifactorial and a number of potential etiological factors have been identified including genetics 5, gender , high mechanical stresses 6 such as heavy lifting 7, vascular insufficiency 8, smoking 9, and
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increased age 2, 6, 10. Further, hypolordosis has been demonstrated to be a potential etiological factor for accelerated DDD in a longitudinal study design 11. MRI has become the most commonly used imaging modality in the diagnosis of DDD. However, the correlation of MRI findings of DDD to clinical symptoms is not fully understood. This might be due to lack of precise observations and documentation of aspects within the complex entity of DDD. This review provides as an overview of the current knowledge regarding MR imaging in DDD, of the diagnostic limitations, and aims to sensitize the reader towards awareness of potentially untended aspects of DDD. A summary of the available classification for DDD is provided.
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MRI protocols of the spine MRI of the spine is generally performed with the patient in supine position. Upright MRI is feasible and favored by some groups due to the plausible explanation that axial loads on the
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intervertebral disc are reduced in supine position and that, as a consequence, dynamic events are ignored per definition with standard MRI. Currently, limited availability of upright MRI,
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its poor resolution, increased motion artifacts and associated high false-positive findings limit widespread use 12. However, a recent study has shown that about one third of patients with
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normal supine MRI had some form of DDD changes in upright MRI 13. Others have demonstrated that upright MRI can provide additional information when dynamic foraminal
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stenosis is suspected 14. Upright MRI with axial loading might be helpful in patients with
with positional pain differences 14.
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clinical symptoms that do not have a morphological correlate in supine MRI 13 or in those
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The standard MRI protocol for DDD typically includes two-dimensional (2D) sagittal T1-
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weighted (T1w) fast spin-echo (FSE), sagittal T2-weighted (T2w) FSE, and axial T2w FSE images. Most institutions add a short tau inversion recovery (STIR) sequence, a gradient echo
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sequence (particularly in the cervical spine) and coronal proton density-weighted (PDw), T2w or T1w sequence. The standard imaging protocols used at the institution of the primary and senior author is summarized in Table 1 and 2. Additional oblique sagittal images may aid in the evaluation of the cervical spine neural foramina, which as a result of their orientation can not be properly assess on standard sagittal images 15. High-resolution three-dimensional (3D) sequences with secondary reconstruction are particularly helpful in the cervical spine. Advantages are that secondary reformatted images can be better oriented along the oblique sagittal plane to show the foramen than standard 2D images and that the higher resolution allows better assessment of the relatively small cervical nerves roots. The latter is especially observed in axial images.
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The sagittal images are used to evaluate the vertebral bodies, intervertebral discs, the ligaments, facet joints, spinal canal and spinal cord and/or sac and intervertebral foramen. The STIR images are usually performed in the sagittal plane as well. Sites of active osteoarthritis
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may be detected on these images. They also provide information of the bone marrow as their fat suppression is usually very homogenous which eases detection of bone marrow changes.
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Axial images are useful for confirmation and evaluation of central canal stenosis, cord signal change, disc herniations, spinal cord compression, and nerve root compression. The facet
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joints are best assessed on axial images for the presence of arthrosis, synovitis and indirectly
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for segmental instability.
The coronal images, if performed, are particularly helpful for identification and classification
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of transitional vertebra, although the osseus bridging transitional vertebra can be identified on a single-slice midsagittal image as well 16. Coronal images also help to get an overview of the
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extent of scoliosis, if present and in detection of extraforaminal herniations.
Gradient echo sequences may be used to evaluate calcification of the ligaments, ossification
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of the posterior longitudinal ligament, and posterior endplate ridges, particularly in the cervical spine. Calcification in general implies as low signal intensity structure, although it can also imply as high signal intensity structure in T1w images, if containing lipids, melanin or bone marrow.
The use of contrast can be helpful in the postoperative setting. Some authors report superior evaluation of disc herniation postoperatively with pre- and early post-contrast images in order to be able to distinguish between epidural fibrosis and disc tissue 17. While there is a diffuse contrast-media uptake in epidural fibrosis/granulation tissue, there is only rim-enhancement in disc tissue 17. Further, partially healed chronic annular tears may demonstrate enhancement due to the presence of granulation tissue, not identified in normal T2w non-contrast MR images . 5
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MR neurography including diffusion tensor imaging (DTI) techniques for the spinal cord and nerve roots are currently only used for specific questions (e.g. in patients with
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neurofibromatosis) and for research, but not yet used in standard protocols 18.
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Intervertebral Disc
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Normal anatomy and imaging appearance
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The intervertebral disc consists of a centrally located nucleus pulposus encircled by the annulus fibrosus, which is attached to the cartilaginous endplates. The annulus fibrosis is a
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strong fibrocartilaginous structure with dense fibers, containing primarily type I collagen. In contrast, the nucleus pulposus is a very soft structure mainly containing water (70-90%) and
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proteoglycans in a loose network of Type II collagen 19. In adults (>30years) in the center of
fibrous plate 20.
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the disc a transversely oriented band of hypointense signal is often visible representing a
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The intervertebral discs of the cervical and thoracic spine are much thinner as compared to the intervertebral discs of the lumbar spine. Further, the annulus fibrosis is thicker in the lumbar spine than in the cervical or thoracic spine 2, 10, 21. The intervertebral disc is mainly avascular and supplied by passive diffusion from the vertebral endplates. In fact, the L4/5 disc space is the largest avascular structure in the body 22. The nucleus pulposus is hypointense compared to the vertebral bodies on T1w images and hyperintense on T2w images due to its high water and proteoglycan content. By contrast, the annulus fibrosus shows lower signal intensities on T1w and T2w images 21. The endplates are well defined and smooth with an intact covering of cortical bone. Age-related changes or agedependent degeneration of the intervertebral disc include mainly decreasing disc cellularity and alteration of the extracellular matrix 23. 6
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Pathologic appearance and features of DDD on MRI
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Dehydration and degeneration of the intervertebral disc Disc degeneration is characterized by presence of dehydration of the disc 24. Disc dehydration
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results from decreased proteoglycans that normally function to bind water. There is a relative
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increase of type I collagen within the nucleus pulposus of degenerated discs 25.
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The disc matrix turnover can be divided in three phases. Phase I is described as growth period (synthesis of aggrecan and procollagens I, II and increased denaturation of type II collagen)
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between 0-15 years of age; phase II (maturation and ageing phase) is characterized by reduction in synthesis (except for type I procollagen) along with reduction in denatured type
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II collagen; phase III (degeneration and fibrotic phase) by increased denatured type II
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collagen and increase in synthesis of type I procollagen (40-80 years) 26.
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On MRI, disc degeneration manifests as loss of intranuclear T2 hyperintensity and subsequent loss of disc height. Pfirrmann et al. classified disc degeneration based on a combination of (a) disc structure, (b) distinction between the nucleus pulposus and the annulus fibrosus; (c) signal intensity and (d) the intertervertebral disc height 27 (Figure 1). Griffith et al modified the Pfirrmann grading system adding three more stages that included a quantitative measurement of the disc height reduction in severe dehydrated discs 28. Newer MR techniques such as T2/T2*- mapping 29, T1-Rho 30, chemical exchange saturation transfer 31, delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) 32, Sodium MRI 33 and Spectroscopy 34 allow evaluation of disc degeneration based on chemical composition of the disc, mainly by evaluation of proteoglycan content. This might result in detection of disc degeneration at an earlier stage 33. However, those techniques are still under development and 7
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not yet included in clinical routine. The main reasons for that are low signal to noise ratios, unavailability on standard MRI scanners or long scanning times 35. Further, more studies are warranted to prove their superiority compared to the Pfirrmann scoring system. Particularly,
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taking into account that early MRI changes often reflects the normal physiologic process of
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aging 36.
Intra-discal gas might be difficult to identify on MRI. The usually impression is that of low
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signal intensity on both T1w and T2w images. When present, intra-discal gas may be seen in association with peripheral annular high signal intensity on T2w images 37. A characteristic
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can however not be appreciated on MR images.
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sign for intradiscal gas is its presence in extension and disappearance in flexion 37. The latter
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Anulus fibrosus tears
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Three forms of annular tears have been described: (a) concentric, (b) radial and (c) transverse tears, however to the knowledge of the authors differentiation of these three forms with the
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use of MRI is challenging. Annular tears have been found in asymptomatic adults, however the concentric tears seem to be more often found in normal discs as compared to transverse tears that are found in degenerative discs 22. Some suggest that annular tears occur early in the course of DDD and may lead to faster development of DDD 38. However a recently performed longitudinal study showed that an annular tear defined as a hyperintensity zone on T2w images within the annulus fibrosus does not accelerate disc degeneration when compared to matched control discs 39. Annular tears are in generally detected by high signal intensity on T2- weighted images (Figure 2). The use of gadolinium might increases the sensitivity for detecting annular tears due to enhancement of granulation tissue within a healing annular tear 40. However in some annular tears the T2w hyperintense signal remains over several years 39 and thus further 8
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studies are needed to evaluate when and which annular tears undergo healing with granulation tissue repair.
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Bulging/Protrusion/Extrusion of the disc In general disc herniation is a result of disc degeneration; herniation without degeneration is
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extrusion is best evaluated using sagittal and axial images.
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rarely seen and typically is caused by extensive traumatic forces. A disc protrusion or
41
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It is important to differentiate between a bulge and a herniation using axial images (Figure 3) . A bulging disc is often seen in asymptomatic individuals and possibly only a consequence
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of normal aging disc. It is further important to differentiate between a protrusion and an extrusion, particularly in case of neural compression. While an extruded disc could be
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surgically removed without need of an annulotomy, a protrusion or bulge needs an
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annulotomy. The distinction between a disc bulge and further between a protruded and extruded herniation is mandatory that surgeons know in advance whether annulotomy and
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nucleotomy is needed or not. Surgical time is increased with the need of an annulotomy and nucleotomy and subsequent faster disc degeneration may occur. The latter has been shown in animal models where DDD was induced by as the means of nucleotomy 42. A disc bulge is a circumferential prolapse of the intervertebral disc (at least >50% of the circumference of the disc) 41, 43 but the annulus fibrosus stays intact. A disc bulge is very often seen in asymptomatic individuals and mostly asymptomatic. A herniation is further differentiated into (a) protrusion, (b) extrusion and (c) sequestration (Figure 3) while a sequestration is correctly defined as a subgroup of an extrusion. Herniations are further described according to the location (central, paracentral, foraminal and extraforaminal) (Figure 4). Some authors prefer the term left or right central instead of paracentral 41. 9
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A protrusion is defined when the protruded disc material extends <50% of the disc circumference and if the size of the base/neck of the protruded material exceeds the maximal length of the protruded material 41, 43. A protrusion can further be classified in focal (<25% of
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the disc circumference) or broad-based (25-50% of the disc circumference) 41, 43. In a protruded disc, at least some fibers of the overlying annulus and posterior longitudinal
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ligament remain intact 37. Surgically, a protrusion might better be classified into the group of disc bulging, as it often needs annulotomy for removal.
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An extrusion is defined if the size of the base/neck of the protruded material is less than the
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maximal length of the protruded material 41, 43. With extrusions and sequestrations, the annulus fibrosus and sometimes the overlying posterior longitudinal ligaments are focally
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disrupted. A free disc fragment or sequestration is defined as a piece of disc that is separated from the original disc. The fragment may migrate superiorly or inferiorly with respect to the
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disc space and rarely may be located intradurally 37.
In addition to location (Figure 4), disc herniations should be described in relation to the nerve
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roots, with particular attention to the degree of nerve contact, displacement or compression 44. Foraminal nerve compression is best evaluated using sagittal T1w images in the lumbar and thoracic spine. A grading system for foraminal nerve compression was introduced by Wildermuth et al 45 (Grade 0: absence of foraminal stenosis; Grade 1:. mild foraminal stenosis (<50%); Grade 2: moderate foraminal stenosis (>50%); Grade 3: severe foraminal stenosis (nerve root collapse)). Nerve roots in the intervertebral foramen are located superior to the intervertebral discs in the lumbar spine. Therefore, a foraminal herniation doesn’t necessarily affect the nerve root. In the lumbar spine a clinically symptomatic nerve irritation/compression is most often cause of multifactorial process (disc herniation, dorsal spondylophtes, flavum ligament hypertrophy and arthrosis of the facets joint). Complete
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absent fat around the nerve root in the intervertebral foramen is consistent with nerve root compression in the lumbar spine. In contrast, in the cervical spine the nerve root at the intervertebral foramen is located at the
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same level or slightly below the intervertebral disc 46. Therefore, small protrusions might already cause symptoms and sagittal oblique or high-resolution 3D- images are of utmost
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importance for the detection of such small protrusions. Maintained fat around the nerve root in the intervertebral foramen is an unreliable sign in the cervical spine. This is also
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demonstrated in a newly introduced grading system for cervical spine foraminal stenosis, using oblique sagittal sequences. There, the authors anecdotally demonstrate the case of a
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patient with only a grade 1 foraminal stenosis suffering from radiculopathy 47.
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A grading system to grade the disc herniation in relation to a recessal nerve root irritation was proposed by Pfirrmann et al 44 for the lumbar spine: Grade 1 describes contact to the nerve
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root without displacement or compression; grade 2 refers to nerve root displacement by disc
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material; and grade 3 encompasses nerve root compression 44 (Figure 5). This grading system has been shown to be reliable with a good interreader agreement for the higher grades
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(comparing grades I- III), but was slightly less reliable in distinguishing normal roots versus grade I (contact) 44.
Indirect signs for nerve root compression are enlargement of the nerve root (pre- and post compression) and nerve root enhancement after gadolinium application. The underlying mechanism for nerve enlargement and enhancement may relate to inflammation and alteration of the blood/nerve barrier 48.
Bone marrow changes of the endplates Endplate changes on MRI were first described in the 1980s and classified into three types by Modic et al according to the underlying bone marrow signal change 49, 50.
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Modic type I changes are manifested as T1w hypointense and T2w hyperintense corresponding to a stress reaction of the bone marrow (Figure 6). Percutaneous biopsies demonstrated the underlying patho-morphological changes namely subchondral fractures and
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vascularized fibrous tissue replacing the hematopoetic bone marrow 49-51. Modic type II changes are seen if the bone marrow undergoes fatty replacement resulting in increased signal
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on T1w and intermediate to high signal on T2w (Figure 6). Modic type III changes are seen as T1 as hypointensities and T2 as hypointensities, reflecting the presence of dense woven
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bone 50 (Figure 6).
can even convert to normal bone marrow 51, 52.
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The progress of Modic changes is not necessarily orderly from I to III, Modic type I changes
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Modic changes seem to be a specific (97%), but insensitive (23%) for painful lumbar disc disease 53. Type I and III changes seem to be more often associated with low back pain (73%)
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than Type II changes (11%) 54.
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Future research focuses towards detection of endplate changes prior to bone marrow changes by direct evaluation of the cartilaginous endplates, e.g. with ultrashort echo time MR imaging or by perfusion evaluation of the endplate 56. Recently, it was reported that perfusion of
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endplates changes using dynamic contrast-enhanced MRI profiles was significantly different if degenerative marrow changes were visible 56.
Interaction of disc degeneration and endplate changes Some authors assume that the disc degeneration may result from initial endplate damage leading to decreased disc nutrition. Changes in diffusion with different degrees of degeneration based on the Pfirrmann classification seem to correlate to a newly introduced endplate damages score 57 (Figure 7). Pfirrmann grades seem also to correlate with the Modic changes 58. However, further studies are required to determine whether the endplate changes cause disc degeneration or vice versa. 12
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Most common levels of degenerative disc disease
Cervical spine
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Disc herniations and Modic changes in the cervical spine are most often observed at C5/6 and C6/7 (Figure 8a) and often reported in young patients (third to fourth age decade) 37. The loss
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of T2w signal hyperintensity of a normal intervertebral disc in T2w images is not as helpful as
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in the lumbar spine for identification of degeneration 37 because the intervertebral disc of the cervical spine is in general of lower signal intensity compared to the lumbar spine (Figure
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8a).
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Thoracic spine
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DDD in the thoracic spine is less common compared to the cervical or lumbar spine. Disc herniation is rare and is most often seen at the level Th11/12 and Th12/L1, most likely due to
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free ending or floating ribs 59 as a result of a lever arm effect of the rigid construct above. Above Th11, the ribs and the sternum serve as a stabilizing construct for the whole thoracic spine, comparable to a fusion 37 and Th1-Th10 vertebra seem therefore less prone to degeneration.
Lumbar spine
DDD of lumbar spine is most observed at the L4/5 and L5/S1 level (Figure 8b). This however does not apply to subjects with lumbosacral transitional vertebrae (LSTV), as the transitional level seems protected as compared to the level above the LSTV, which is prone to DDD 60. This observation has been observed particularly in higher type of LSTV according to the Castellvi Classification, where posterior osseous bridging limits segmental motion 60. 13
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Conclusion
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MRI is the most commonly used imaging modality in diagnosis of DDD. Standard MRI is performed in the supine position and cannot reflect dynamic aspects of DDD. Classifications/
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grading systems of DDD and associated pathologies such as endplate changes or affection of
neural structures are described and should be used in order to quantify DDD and differentiate
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the complex entity of DDD. The differentiation of disc bulging and herniation is of immediate
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clinical and surgical relevance while protrusion of the disc should better be classified as a form of disc buldging rather than disc herniation, as if surgically treated, former needs often
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surgical annulotomy.
Lack of precise observations and documentation of aspects within the complex entity of DDD
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might partially be the cause of poor correlation of radiographic finding to clinical symptoms.
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Legend to the figures
Figure 1. Examples of the different grades of lumbar disc degeneration according to
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Pfirrmann et al 27. Schematic and corresponding T2w sagittal MR images show (a) grade Ihomogenous, bright hyperintense disc structure and a normal disc height, (b) grade II-
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inhomogenous, but hyperintense disc structure with clear differentiation between nucleus and
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annulus and normal disc height, (c) grade III- inhomogenous, intermediately gray disc with an unclear distinction between nucleus and annulus, the disc height is normal or slightly
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decreased, (d) grade IV- inhomogenous, hypointense dark-gray disc with a lost distinction between nucleus and annulus and with the disc height normal or moderately decreased, (e)
annulus and a collapsed disc space.
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grade V- inhomogenous, hypointense black disc with lost distinction between nucleus and
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Note: Pfirrmann classification was described using T2w sagittal FS FSE sequences (TR/TE
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5000/130). Our lumbar spine protocol is performed with TR/TE: 5000/93 and note that not all
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of the here represented images were performed with FS.
Figure 2. Example of an annular tear. (a) Sagittal and (b) axial T2w FSE show a hyperintense disruption of the annulus paracentral on the right side (arrow). Note the recessal nerve root deviation on the same side (arrowhead)
Figure 3. Schematic illustration and the corresponding axial T2w FSE MR images of disc a) bulging (arrows), b) protrusion (arrows), c) extrusion (arrow) and d) sequester (arrow). The signal of the sequestered fragment changes slightly to hyperintense with progression and the
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fragment may migrates, in this case the fragment is located above the disc level, on the level of the next vertebral body. Note that the neck/base of an extruded disc is equal or smaller than the maximal length of the extruded disc material in contrast to a protrusion where the
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neck/base exceeds the maximal length of the protruded material.
Figure 4. (a) Schematic illustration of potential locations of a disc herniations in the axial
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plane. T2w FSE MR images of a (b) median/central disc extrusion (arrow), (c)
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paracentral/recessal broad based protrusion (arrow), (d) foraminal broad based protrusion
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(arrow) and (e) an extraforaminal disc herniation (arrow).
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Figure 5. Schematic Illustrations and corresponding axial T2w FSE MR images of different
44
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grades of nerve root compromise recessal due to disk herniation described by Pfirrmann et al , here slightly modified. a) a median to paracentral disc herniation (a broad-based protrusion
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on the MR-image) without contact to the nerve root (arrow). The epidural fat layer and cerebrospinal fluid between the nerve root and the herniation is preserved. b) Median to paracentral disc herniation (an extrusion on the MR-image) with contact to the nerve root, but without a relevant displacement (arrow). c) Paracentral disc herniation (a broad-base protrusion on the MR-image) with displacement of the recessal nerve root dorsally (arrow). d) Large paracentral disc herniation (an extrusion on the MR image) with recessal nerve root compression due to the disc herniation against the wall of the spinal canal (arrow).
Figure 6. Sagittal T1w and T2w MR images show the different types of Modic changes 50. Type I, represents bone marrow edema (T1w hypointense, T2w hyperintense); type II, 24
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represents fatty bone marrow replacement (T1w hyperintense, T2w hyperintense); type III,
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represents presence of dense woven bone (T1w hypointense, T2w hypointense).
Figure 7. Example of the severity of the endplate damage, scored according to Rajasekaran et
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al 57. Schematic and corresponding sagittal T1w FSE images show (a) type I- normal
endplate, with no interruption, (b) type II is a thinning of the endplate, no obvious break, (c)
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type III is a focal endplate defect with established disc marrow contact but with maintained
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endplate contour, (d) type IV is defined as endplate defects less than 25% of the endplate area (arrow), (e) type V is defined as endplate defects up to 50% of the endplate area (arrow and
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arrow head in (d)), (f) type VI is defined as extensive damaged endplates up to total
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destruction. Type IV-VI are often associated with Modic changes in the bone marrow.
Figure 8. T2w FSE MR images show typical locations for disc degeneration in the (a)
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cervical spine at the levels C5/6 and C6/7 (*) and in the lumbar spine at the levels L4/5 and L5/S1 (*).
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Tables Table 1. MR protocol lumbar spine on 1,5T scanner Sag T1w Sag T2w Sag STIR FSE FSE
Axial T2w FSE
Coronal T2w FSE
500
5000
3600
4000
4500
TE
9.5
95
35
101
101
3
3
3
123
32
18
22
NEX
1
1
1
FOV (mm)
280
280
280
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3
3
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Slice thickness (mm) ELT
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TR
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1
220
1
280
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307 x 384 336 x 448 288 x 320 336 x 448 288 x 384 Matrix Spacing 0.6 0.6 0.6 0.3 0.6 (mm) Sag, sagittal; T1w, T1-weighted; FSE, fast spin-echo; T2w, T2-weighted; STIR, short-tau inversion recovery; CM, contrast media TR, repetition time; TE, echo time; ETL, echo train length; NEX, number of excitations; FOV, Field of view.
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Table 2. MR protocol cervical spine on 1,5T scanner Sag T1w FSE
Sag T2w FSE
Sag STIR
Axial T2w Sag oblique FSE T2w FSE
3D GRE
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690 3500 4000 3500 3500 532 TR 9.5 126 39 91 131 15 TE 3 3 3 3 2.5 3 Slice thickness (mm) 135 30 18 10 26 ELT 2 1 3 3 1 3 NEX 220 220 220 160 220 160 FOV (mm) 269 x 384 307 x 512 269 x 384 240 x 320 269 x 448 256 x 256 Matrix 0.3 0.3 0.3 0.1 0.1 0.3 Spacing (mm) Sag, sagittal; T1w, T1-weighted; FSE, fast spin-echo; T2w, T2-weighted; STIR, short-tau
inversion recovery; CM, contrast media TR, repetition time; TE, echo time; ETL, echo train
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length; NEX, number of excitations; FOV, Field of view.
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Acknowledgments:
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The authors thank the University Hospital of Zurich for providing the MR images used in this article and the Swiss National Fond who supported individual funding of Nadja A. FarshadAmacker.
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Highlights
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1. This systematic literature review summarizes the current knowledge on MR imaging in degenerative disc disease. 2. Different classification systems for segmental spine degeneration are summarized. 3. It outlines the diagnostic limitations of MR imaging.
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