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387

Tractography: Possible Applications in


Musculoskeletal Radiology
Anne Cotten, MD, PhD1,2 Farah Haddad1 Georges Hayek, MD1 Guillaume Lefebvre, MD1
Emilie Dodré, MD1 Jean-François Budzik, MD, PhD1,2,3

1 Service de Radiologie et Imagerie Musculosquelettique, Centre de Address for correspondence Anne Cotten, MD, PhD, Service de
Consultations et d’Imagerie de l’Appareil Locomoteur (CCIAL), CHRU Radiologie et Imagerie Musculosquelettique, Centre de Consultations
de Lille, rue du Pr Emile Laine, Lille Cedex, France et d’Imagerie de l’Appareil Locomoteur (CCIAL), CHRU de Lille, rue du
2 EA4490-PMOI, Université du Littoral-Côte d’Opale, Laboratoire de Pr Emile Laine, 59037 Lille Cedex, France
Physiopathologie des Maladies Osseuses Inflammatoires, Boulogne (e-mail: anne.cotten@chru-lille.fr).
sur Mer Cedex, France
3 Imagerie Médicale, GHICL, Hôpital St-Vincent-de-Paul, Lomme,
France

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Semin Musculoskelet Radiol 2015;19:387–395.

Abstract Tractography (or fiber tracking) consists of three-dimensional modeling of the prefer-
ential movement of water molecules in the form of fiber tracks from the tensor field
information. This technique allows a new approach for the microarchitectural analysis of
Keywords anisotropic structures such as nerves, white matter, and muscles. Many disorders have
► diffusion tensor been studied including cervical myelopathy, carpal tunnel syndrome, nerve root
imaging compression, and nerve tumors. Muscles have been less evaluated. Tractography is
► diffusivity still a research technique, and its validation and widespread routine clinical use will
► fractional anisotropy require a good deal of work toward a harmonization of the MRI protocols and data
► tractography postprocessing methods.

Diffusion Imaging and Diffusion Tensor tion about the orientation and architectural organization of
Imaging the tissue.
Diffusion tensor imaging (DTI) allows this assessment. DTI
Diffusion imaging demonstrates the random diffusion of is a further development of the previous technique that
extracellular water molecules in tissue. This is usually accom- applies gradients in at least six directions. The purpose is to
plished through the use of spin-echo single-shot diffusion- obtain more precise information not only regarding the
weighted echo-planar imaging with a bipolar diffusion-en- overall diffusion of water inside the tissue, but also regarding
coding gradient in three directions. The apparent diffusion its preferred direction. The higher the number of directions
coefficient (ADC) quantifies water molecules displacement along which the diffusion gradients are applied, the more
and as a consequence provides indirect information about the precise the determination of anisotropy. However, a large
structures surrounding these molecules. Such diffusion can number of directions increases the acquisition time and
be isotropic, with the movement of water molecules occur- therefore the motion blur.1 In fact, the choice of this number
ring freely in all directions in space, or anisotropic, with the depends on the structure to assess because six directions can
overall diffusion of water molecules occurring in a preferred be enough for a median nerve, which has a vertical direction,
direction. In highly ordered tissues such as the spinal cord and but 15 to 25 directions can be required for a brachial plexus.
nerves, the molecular motion of water preferentially occurs The b factor expresses the power of the diffusion gradients
along one axis, the axis of the axons, with much less motion in in seconds per millimeter squared. When b increases, the
a direction perpendicular to that axis. As a consequence, power of the gradients increases, the diffusion weighting of
measuring anisotropy of these structures provides informa- the sequence increases, but the signal-to-noise ratio, which is

Issue Theme Update on Advances in Copyright © 2015 by Thieme Medical DOI http://dx.doi.org/
Musculoskeletal Magnetic Resonance Publishers, Inc., 333 Seventh Avenue, 10.1055/s-0035-1563736.
Imaging; Guest Editor, Patrick Omoumi, New York, NY 10001, USA. ISSN 1089-7860.
MD, MSc, PhD Tel: +1(212) 584-4662.
388 Tractography Cotten et al.

critical in fiber tracking, decreases. So this choice is impor- for fiber tracking. The main ones are the FA threshold value,
tant. In general, the b values used for musculoskeletal imaging the b0 threshold value (allowing the elimination of noise), the
are frequently  700 to 1,000 s/mm2. A compromise thus has angulation threshold of the fiber, and its minimal length. As a
to be found between a good signal-to-noise ratio, good spatial rule, the software uses a combination of several of these
resolution, and an acceptable acquisition time. The balance parameters to display the fibers. Once the tractography
between the diffusion-specific parameters and those com- algorithm has been launched on the FA mapping, it is thus
mon to all MRI sequences is essential for the achievement of possible to obtain a 3D modeling of the structure under study.
DTI images that allow efficient and reliable postprocessing of The color coding is the same as that used in FA maps, and
data. anatomical fusion with T1- or T2-weighted sequences allows
The diffusion gradients applied in at least six directions us to estimate the relevance of the reconstructions. The
provide information on the diffusion inside each voxel exam- volume under study can then be manually restricted to the
ined. This can be schematized by a three-dimensional (3D) structure of interest. The structure is then analyzed with
ellipsoid formed because of three main vectors, each having FiberViewer software, which can provide the DTI measure-
its own magnitude, in the dominant direction and in the two ments along the structure on a curve.
perpendicular directions. In simpler terms, the preferred Measuring these DTI parameters with a FiberViewer on
diffusion directions can be depicted by mappings using a tractography images rather than using region of interest (ROI)

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specific color code initially used in neuroradiology such as on FA maps probably does not change much for large and
blue for the craniocaudal direction, red for the left-to-right vertical structures such as the median nerve, but for the
direction, and green for the anteroposterior direction. These assessment of thin or complex structures such as the lumbar
maps can be superimposed with corresponding anatomical nerves or the brachial plexus, this can be particularly useful.
images. For example, in the presence of a compressed lumbar nerve by
DTI parameters can be calculated voxel by voxel using a disk herniation, you need to avoid partial volume effects, but
software applications such as MedINRIA. These are the two you need sufficient information, which of course will be a
main parameters: problem at the level of the nerve root compression. Tractog-
raphy allows the nerve to be followed at the level of the
-Overall diffusivity, which can be expressed either by
compression and the microstructural parameters to be mea-
means of ADC or in terms of average diffusivity. The
sured along the course of the nerve. This explains why
more obstacles the molecules encounter, the less they
measurements of DTI parameters may be more reliable on
move and the weaker the diffusion. This diffusivity corre-
tractography than by using ROI, at least for some structures.7
sponds to the following mathematical formula: λ ¼ (λ1þ
λ2þ λ3)/3.3–5 Diffusivity can be divided into axial diffusiv-
ity, designated by λ1 (the magnitude of the dominant Spinal Cord
direction), and radial diffusivity designated by (λ2þ λ3)/
The white matter of the spinal cord is made up of well-
2, the average magnitude of the two other directions.
arranged clusters of nerve fibers, vertically oriented, whose
Differentiating between these two types of diffusion can
anisotropy is therefore marked (far more so than that of the
be useful, especially when evaluating nerves and white
gray matter).8 MRI is the imaging modality of choice for the
matter.6
assessment of cervical spondylotic myelopathy. However,
-Fractional anisotropy (FA), which quantifies the direction-
abnormal signal intensity of the spinal cord, especially on
al dependence of water diffusion. The values range from 0
T2-weighted images, is poorly correlated with the clinical
to 1. The higher the FA, the more the water molecules will
symptoms, because it may be noticed in various lesions
be “forced” to diffuse in a preferential direction. A high FA
whose severity varies greatly.9,10 Tensor diffusion imag-
usually indicates good integrity of the structure.
ing11–14 and tractography15 have enabled the evidence of a
To obtain these parameters, cross-sectional area measure- change in the microarchitectural parameters of the spinal
ments can be calculated on the FA maps. cord, even when no abnormal spinal cord signal is detected on
conventional sequences. The drop in FA, which appears to be
more sensitive than the increase in mean diffusivity
Tractography
(MD),15,16 appears to be correlated in tractography with
Tractography (or fiber tracking) is a powerful extension of the the severity of the clinical impairment,15,17,18 even though
previous technique. It consists of 3D modeling of the prefer- not all teams have observed this14 (►Fig. 1). We may suppose
ential movement of water molecules in the form of fiber that in case of edema, the spinal cord retains its fibrillar
tracks from the tensor field information. The fibers’ tracking architecture (the drop in FA is not marked), in contrast with
and display criteria vary according to the software used. In medullary necrosis and cavitation, accompanied by an FA
our department, we use MedINRIA, which allows tractogra- drop because water can diffuse much more freely. And this is
phy of the entire volume obtained with MRI. The aim of the particularly important, as the predictive value of DTI regard-
software is to interconnect voxels having similar main vectors ing postoperative outcome has been reported.19 The alter-
and FA values, on the assumption that voxels whose proper- ations of the visual aspect of the tractography (normal,
ties are comparable belong to the same tissue (line propaga- indentation, partial or complete interruption) and the num-
tion method).1 Several parameters may be taken into account ber or length of the fibers counted by the software have been

Seminars in Musculoskeletal Radiology Vol. 19 No. 4/2015


Tractography Cotten et al. 389

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Fig. 1 Cervical spondylotic myelopathy in a 59-year-old woman with severe functional impairment. (a) Sagittal T2-weighted image shows
increased signal intensity of the spinal cord. (b) Interruption of fibers (suggesting the tissue became isotropic) and spinal narrowing on the
diffusion tensor imaging-fiber tractography image. (c) Blown-up image of the tractography in the area of compression with an important
fractional anisotropy (FA) drop at the compressed site on the FA histogram. (d) The segmented spinal cord. Fig. 1a–c reprinted with permission
from reference 15.

Fig. 2 Tractography of the median nerve inside the distal carpal


tunnel in a volunteer.

diversely correlated with the severity of the clinical damage


and with the patient’s prognosis; to date, the results are still
unconvincing.16,20,21
Tractography-based DTI measurements can also quantify Fig. 3 Postsurgical neuroma affecting the three-dimensional visuali-
the degeneration of specific tracts of white matter.22 This zation of the median nerve fibers. The mass effect of the disk
specific assessment might allow depiction of more subtle herniation is clearly demonstrated.

Seminars in Musculoskeletal Radiology Vol. 19 No. 4/2015


390 Tractography Cotten et al.

changes or unilateral abnormalities that can not be detected (►Fig. 2), the frequency of disorders affecting it at the wrist,
by the assessment of the whole cord. and the ease of its electroneurologic and MRI evaluation.
Tensor diffusion imaging and tractography have also been
used to evaluate other disorders of the spinal cord (traumatic Carpal Tunnel Syndrome
lesions, tumors, arteriovenous malformations, myelitis, com- In patients presenting a carpal tunnel syndrome, most au-
pression, diastematomyelia, and attached long spinal cord), thors have reported a decrease in FA.2,23–27 However, FA
but most of them are evaluated by neuroradiologists. varies along the carpal tunnel; it tends to increase distally
in controls (as the fibers go through a smaller space) and to
decrease in patients (intrafascicular edema).23,28,30 An anal-
Peripheral Nerves
ysis of the difference between the distal and proximal meas-
The peripheral nerves also represent strong anisotropic struc- urements could thus increase the sensitivity of the results.
tures. The median nerve is the most studied peripheral nerve However, an unchanged value23–25,27 or an increase in
in the literature due to its large caliber, its rectilinear course ADC2,24,29 has also been reported in the literature.

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Fig. 4 Tractography of the right S1 root with anatomical correspondence in a patient with a right posterolateral disk herniation. The mass effect is
clearly seen on the (a) lateral and (b) frontal views. The fractional anisotropy can be measured along the compressed nerve root, the blue mark
showing the part of the nerve being measured (c). Fig. 4a, b reprinted with permission from reference 7.

Seminars in Musculoskeletal Radiology Vol. 19 No. 4/2015


Tractography Cotten et al. 391

The apparent heterogeneity of these results may be ex- Spinal Nerves


plained by the diversity of the protocols used, but also by the A decrease in FA and an increased diffusivity in cervical or
varying severity of the carpal tunnel syndrome. Indeed, even lumbar nerve roots compressed by a disk herniation have
if a good correlation has been reported between the changes been reported in the literature (►Fig. 4).37–39 Similar changes
in the DTI parameters and the electroneurography in DTI parameters were also reported in patients with nerve
data,24,29–31 this type of measurement seems to lack sensi- root pain in the absence of compression.38 These parameters
tivity to detect moderate nerve compressions.23,29 Moreover, could thus be correlated with the clinical data, regardless of
a great variability of the diffusion parameters has been the existence of a nerve root compression.38 In a recent
reported in normal subjects,28,32,33 which explains why it study,37 the clinical data were correlated with MD and axial
is difficult to define a threshold value enabling a distinction and radial diffusivity values, but not with FA values, suggest-
between health and disease. Finally, these parameters must ing that demyelination, axonal swelling, and edema or in-
be analyzed according to the age of the patient. Indeed, flammation of the adjacent tissues are more responsible for
changes in diffusion and anisotropy similar to those observed the symptoms observed in the case of nerve compression
in carpal tunnel syndrome may develop with age, in the than the alteration of axonal density. Tractography can also
absence of any clinical symptoms.2,28,29 Conversely, the sex perfectly demonstrate a mass effect, a narrowing or complete
of the patient does not seem to influence the values of the interruption of the tracted root, but its contribution as

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diffusion parameters. compared with classical morphological sequences remains
A single study has focused on the recurrence of carpal to be specified. This imaging method could, however, perhaps
tunnel syndrome after surgery.30 Patients showed a decrease prove useful to reveal evidence of extraforaminal nerve
in diffusion, but the FA, which quantifies the structural compression.40 The achievement of a good quality tractog-
integrity of the nerves, was intact. In addition, those with raphy of lumbar roots at 3 T is fostered by the use of reduced
endoneurial fibrosis (defined by an enlarged median nerve fields of view to avoid some artifacts such as distortion of the
and endoneurial enhancement after gadolinium injection) dural sac, which are more pronounced at this magnetic
had lower ADC and radial diffusion values than those without field.41
fibrosis. Endoneurial fibrosis may thus impede the free
diffusion of water but also affect the myelin rather than the Brachial and Sacral Plexus
axon because axial diffusion, which informs about axon DTI-derived measurements and fiber tractography of brachial
integrity, was less affected (intrafascicular scar).34,35 The plexus has been described in volunteers,42 but its usefulness
usefulness of the 3D visualization of the median nerve by in pathology has not been studied extensively (►Fig. 5). The
this technique has not yet been fully assessed (►Fig. 3). sacral plexus may also be tracked up to the root of S3 and to
the pudendal nerve, with possible involvement in the evalu-
ation of spina bifida with neurogenic bladder.43 A truncated,
Other Nerves
irregular, and disorganized appearance of roots S1 to S3 with
Ulnar Nerve a decrease in FA has also been reported in women with
The ulnar nerve at the cubital tunnel has been evaluated less painful pelvic endometriosis,44 suggesting associated proxi-
often. Interestingly, discontinuity of the nerve proximal to the mal microstructural nerve injury, and may perhaps partially
medial epicondyle, indicating a more proximal compression explain the possibility of persistence or recurrence of pain
than in the cubital tunnel, has been reported.36 after surgical removal of the pelvic endometriosis lesions.

Fig. 5 Tractography of the roots of the brachial plexus.

Seminars in Musculoskeletal Radiology Vol. 19 No. 4/2015


392 Tractography Cotten et al.

Particular Indications

Axonal Degeneration and Regeneration


The studies published in the literature have mainly focused on
animal models. In case of injury to the sciatic nerve by
compression or stretching, FA decreases during the phase
of Wallerian degeneration and increases during the regener-
ative phase.45–47 Tractography may represent an attractive
means of visualizing nerve interruption and its regeneration
over time.46,48

Tumors and Pseudotumors


The 3D depiction of nerves in tractography could also
be used to study the relationship between a lesion and
a nerve structure, particularly when planning surgery
(►Figs. 6 and 7). Some authors have reported a higher

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frequency of interruption or complete disorganization of
the fibers in case of malignant tumors, whereas benign
tumors are more often associated with a normal appearance,
a deviation, or a partial interruption of the fibers.49–53
However, it is important to recall that we are dealing with
functional imaging and not with direct anatomical imaging.
Therefore, areas of axonal degeneration and/or associated
loss of myelin may result in a focal loss of fibers, whereas the
fasciculate anatomical architecture may still be preserved.

Muscle
Muscle has been less studied in DTI and tractography
Fig. 6 Tractography of a cystic schwannoma of the ulnar nerve. Note
the eccentric location of the tumor. (►Fig. 8). Certain histologic features explain the necessary

Fig. 7 (a) T2-weighted image and (b) tractography of the relationship between the proximal aspect of a schwannoma and the tibial nerve (patient with
neurofibromatosis type 2). Note the eccentric location of the tumor.

Seminars in Musculoskeletal Radiology Vol. 19 No. 4/2015


Tractography Cotten et al. 393

Conclusion

Tractography can provide beautiful 3D images and enable


precise objective measures in terms of microstructural
changes of nerves, white matter, and muscles. But this is still
a research technique, and its validation and widespread use in
clinical routine will continue to require a good deal of work
for the harmonization of MRI protocols and data postprocess-
ing methods.

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