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ISSN: 0309-1902 (print), 1464-522X (electronic)

J Med Eng Technol, 2014; 38(1): 14


! 2014 Informa UK Ltd. DOI: 10.3109/03091902.2013.844207

INNOVATION

MR-based measurement of spinal cord motion during flexion of the


spine: implications for intradural spinal cord stimulator systems
S. Viljoen1, C. A. Smittkamp2, B. D. Dalm1, S. Wilson1, C. G. Reddy1, G. T. Gillies3, and M. A. Howard III*1
1
Department of Neurosurgery, 2Department of Radiology, University of Iowa Hospitals and Clinics, Iowa City, IO 52242, USA, and 3Department of
Mechanical and Aerospace Engineering, University of Virginia, Charlottesville, VA 22904, USA

Abstract Keywords
This study develops a means of delivering electrical stimuli directly to the pial surface of the Dorsal root entry zone, intradural implants,
spinal cord for treatment of intractable pain. This intradural implant must remain in direct neuromodulation, spinal cord, spinal cord
contact with the cord as it moves within the spinal canal. Therefore, magnetic resonance stimulator
imaging was used to measure the movement of the spinal cord between neutral and flexed-
back positions in a series of volunteers (n 16). Following flexion of the back, the mean change History
in the pedicle-to-spinal cord dorsal root entry zone distance at the T10-11 level was (8.5  6.0)
mm, i.e. a 71% variation in the range of rostral-caudal movement of the spinal cord across all Received 24 April 2013
patients. There will be a large spectrum of spinal cord strains associated with this observed Revised 3 September 2013
range of rostral-caudal motions, thus calling for suitable axial compliance within the electrode Accepted 8 September 2013
bearing portion of the intradural implant.

1. Introduction and background titanium strap (termed the Oya Strap) that is secured to the
lateral margins of the boney spinal canal. The dura is closed
A limiting factor in the efficacy of epidural spinal cord
underneath the Oya Strap, forming a water-tight seal that
stimulation for the treatment of intractable pain is the inability
prevents CSF leak. The restoring forces in the compressed
of the standard devices to selectively modulate the targeted
lead loops inside the subdural space create a gentle pressure
neural fibres without inadvertent stimulation of neighbouring
on the electrode membrane [4] (515 mm Hg, which is within
non-targeted structures, e.g. the dorsal nerve rootlets. This is a
the range of normal intrathecal pressures) to keep it in contact
consequence of the shunting effects of the relatively high
with the spinal cord as it moves within the spinal canal. It is
conductivity CSF located between the epidural electrodes and
important that this membrane remains stably in place and
the spinal cord surface, migration of the leads following
does not lift off the surface during rostral-caudal displacement
implantation, the formation of epidural scar tissue and several
of the cord or slide laterally from its midline position, the
other such problems. The result is limited therapeutic efficacy
latter to prevent potentially harmful contact with the dorsal
in up to half of all patients having a standard epidural stimulator
root entry zones (DREZ).
[1]. The Human Spinal Cord Modulation System (HSCMS) is
being developed to improve this situation. It is an intradural
Therefore, the lead loops of the device must be designed 13
20
such that they accommodate all of the relative motion
device [2] placed via durotomy directly onto the pial surface of
between the implant on the spinal cord surface and the lead
the spinal cord, thus avoiding the electrical shunting effects of
exit point which is at a fixed position at the dural exit site
the CSF and lead migration issues and enabling more focused
under the Oya strap. Moreover, the membrane must conform
delivery of the stimulus currents into the targeted regions [3].
to the shape of the dorsal surface of the spinal cord in order
The design features of the wired version of the implanted
for the electrodes to make uniform direct contact with the pial
component of this device are shown in Figure 1. The electrode
surface. This means that the radius of curvature of the
bearing surface at the bottom of the device makes contact
membrane must closely approximate that of the oval-shaped
with the dorsal surface of the spinal cord. It consists of a thin
spinal cord. It should also subtend as large an angle as
membrane (0.6 mm thick) of silicone into which are
possible of the dorsal arc, while leaving a small buffer zone
embedded six stimulating electrodes. The individual leads
on either side that separates the lateral edges of the membrane
from the electrodes are configured in loops which join to form
from the dorsal rootlets. These requirements call for know-
a single lead cable that exits the spinal canal. This cable is
ledge of (1) the spinal cords thoracic morphology and (2) its
held in a stable position relative to the spinal canal by a
axial motion within the spinal canal as a function of spinal
flexion. The first point was addressed via direct image-based
*Corresponding author. Email: matthew-howard@uiowa.edu determination of the inter-DREZ dorsal arc lengths found
2 S. Viljoen et al. J Med Eng Technol, 2014; 38(1): 14

between spinal nerve dorsal root entry zones, a CISS sequence


was selected for its high spatial resolution. Although this is a
highly T2-weighted sequence, acquisition time still required
2 min 5 s. This length of time initially caused too much motion
degradation during flexed imaging to make accurate measure-
ments. The use of the pillows and foam wedges provided just
enough support for volunteers to remain still and in a state of
quiet respiration for the required 2 min duration. This
minimized breathing-related artifacts which, like the residual
motions induced by the cardiac cycle, otherwise limit the
imaging resolution that can be obtained. Hence, the measure-
Figure 1. Artists rendering of the HSCMS device. The 1.5 cm long ments we have are technically an average during quiet
electrode-bearing silicone membrane at the bottom of the device is
placed onto the pial surface of the spinal cord. The leads from the
respiration. All neutral and flexed sequences were obtained
electrodes loop upwards, three per side, to meet and exit as a bundle utilizing TR 4.35 ms, TE 2.18 ms, slice thick-
through the titanium Oya Strap which serves as the fixation structure for ness 0.8 mm, matrix size 192  192, one acquisition per
the device, attaching it to the surrounding vertebra. A dural seal (not average, 192 phase encoding steps, field of view 200 mm and
shown) encloses the lead loops and membrane within the dura and allows
for leak-free passage of the lead bundle through the exit port on the Oya a 70 flip angle.
Strap. An implantable pulse generator (not shown) is located in a nearby
subcutaneous pocket. The lead bundle connects to it and conveys the 2.3. Measurement algorithm
electrical stimuli to the electrodes.
Imaging was obtained in the coronal plane. Three-dimen-
sional multiplanar reconstruction software was utilized on a
across a large number (n 50) of patients [5]. The present Carestream PACS station to aid in measurement. The T10 and
study addresses the second point through implementation of T11 nerve roots were identified. A cranial caudal measure-
an experimental protocol aimed at measuring the flexion- ment was made in a plane parallel to the spinal canal between
driven rostral-caudal movement of the spinal cord. the DREZ of T10 and T11. (The exact position of the entry
zones was confirmed by assessing sequential axial images to
2. Materials and methods
identify the most cranial aspect of the nerve originating from
2.1. Patient position within the magnet the spinal cord.) As shown in Figure 2, the difference between
In order to allow for spinal flexion during imaging, a 1.5 T this measurement on the neutral and flexed images is a
Magnetom Espree (Siemens, Erlangen, Germany) magnet was measure of spinal cord contraction/expansion along the
utilized to take advantage of its larger bore size, which was rostral-caudal axis. Next, a cranial caudal measurement was
designed to accommodate bariatric patients. Informed consent made from the DREZ of the T10 nerve root along the same
was obtained from a total of 16 healthy volunteers ranging in plane as the prior measurement, to the level of a plane
age from 2358. Each volunteer was first imaged in a supine orthogonal to the spinal canal at the level of the inferior T10
neutral position and then imaged in a maximal attainable flexed pedicles. The latter were selected as a reference point of the
position. To obtain the maximal flexion of the spine, patients bony canal inside of which the spinal cord moves. The
were given three basic positioning instructions. The first was to difference between these measurements represents cord
rotate their hips/pelvis backwards towards the gantry as far as movement within the bony canal. An example of a coronal
possible to remove the lumbar lordosis and straighten the image on which the relevant anatomical features are identified
lumbar spine. The second was to curl their upper back, neck and is shown in Figure 3.
head forward so that their shoulders were as close to their knees Lastly, a cranial caudal measurement of the change in
as possible. The third instruction was then to tuck their chin conus tip position was made. In order to accurately accom-
down as close to their chest as possible. While attaining this plish this, the position of the conus tip was first identified on
flexed position in the bore, a variety of foam wedges and the neutral images with reference to a landmark within the
pillows were utilized for added support so that the patient could bony spinal canal at the same cranial-caudal level. This
remain as still as possible during image acquisition. Maximal landmark was then identified on flexed imaging and a cranial
flexion was limited by volunteer flexibility in 14 of the patients. caudal measurement was made from that level to the level of
In only two patients was flexion limited by MR bore size. Not the new conus position. This measurement also represents
surprisingly, these were also the two tallest patients with movement of the spinal cord within the canal.
heights of 2.03 and 1.98 m (60 800 and 60 600 ).
3. Results
2.2. Imaging protocol
The spinal cord should move rostrally during flexion and
Each volunteer had a vitamin E capsule taped to their midline should lie in its most caudal location when the patient is in the
lower thoracic spine for help in level localization. A sagittal neutral position. The measured change in the pedicle-to-spinal
HASTE sequence was performed initially as a localizer both for cord DREZ distance across all patients between the neutral
vertebral level counting and identification of a more focal field and flexion positions ranged from 1.918.0 mm, with a mean
of view centred over the region of lowest thoracic spinal nerves and standard deviation of 8.5  6.0 mm. The inter-DREZ
and the conus medullaris. In order to acquire anatomic images distance across all patients between the neutral and flexion
with enough resolution to accurately measure intervals positions ranged from 2.06.7 mm, with a mean and
DOI: 10.3109/03091902.2013.844207 Measurement of spinal cord motion 3

mean) are very large, 71%, 74% and 64%, respectively. This
reflects the wide variability in the capacity of individual
subjects to maximally flex the spine, as well as possible inter-
subject variability in spinal cord mechanical characteristics.

4. Discussion
Several previous studies have reported both gross anatomical
and image-based measurements of spinal cord motions and
related mechanical parameters, some of which are relevant to
the HSCMS design issues discussed above. For instance,
Figley and Stroman [6] found that the amplitude of the
cardiac-driven pulsation of the anterior-posterior (A/P) com-
ponent of bulk cord movement in 10 immobile patients was
0.60  0.34 mm in the cervical and upper thoracic region.
However, as found in their subsequent study on eight
immobile patients [7], this value was 50.10 mm in the
lower thoracic region (T4/T5 and below), with excursions of
the same size along the left/right axis, thus setting the lower
limits on the size of bulk cord motions in those directions.
Much larger changes (millimetre-scale) in the A/P position of
the spinal cord relative to the dura were found in patients who
Figure 2. The white line running transversely is at the base of the purposely changed posture or carried out flexion/extension
pedicle. The yellow vertical line (on the right) represents the distance manoeuvres during imaging [8,9]. See also the reviews of
from there to the DREZ. The change in that length represents how much Harrison et al. [10] and Cox [11]. Furthermore, it has long
the cord slides during flexed and neutral positions. The green vertical
line (on the left) indicates the inter-DREZ distance and represents how
been known that flexion and extension of the spine produces
much the cord stretches. centimetre-scale axial stretching motions of the spinal cord
and dura along the rostral-caudal (R/C) direction relative to
the other structures forming the spinal canal [12]. However,
that work was carried out on fixed-tissue samples from
cadavers and there are no reported equivalent series of in vivo
measurements that use a similar protocol. While all of these
studies have provided very useful background information, an
effort focusing specifically on determination of the axial
component of spinal cord motion within the region targeted
for HSCMS implantation was needed to complete the picture.
Moreover, from a biophysical perspective, the findings
presented here can also be used to yield the ratio of the spinal
cords mean stretch-to-mean axial movement over a full
flexion cycle: 3.5 mm/8.5 mm &40%. That is, on average
across all patients, it required 1 mm of net axial displacement
of the cord to stretch it 0.4 mm in length. However, as
discussed above, there were large variations between patients
and this makes it difficult to draw generalized conclusions
about the mechanics of the spinal cord in relation to certain
aspects of its interaction with the HSCMS. For instance,
estimates of the net strain within its parenchyma will depend
strongly on the assumptions made regarding how the spinal
cords stretch is distributed over its length, as that will be
governed at least in part by the anisotropies in its structure in
Figure 3. Coronal image on which the nerve-root sheath exit zones are
a given patient. In the worst case, for some patients, high
identified by orange arrows (dark arrows, three on each side), the pedicle levels of parenchymal strain could mean that the HSCMS
locations are marked by blue arrows (light arrows, three on the left side), electrodes might slide across the spinal cords surface unless
and two of the pedicle cross-sections are outlined in blue (the two light the membrane is compliant enough to accommodate this
traces on the right).
component of the cords axial motion. On the other hand, in
those cases where the stretching component is more localized
standard deviation of 3.5  2.6 mm. The mean and standard within a given region of the typically 45 cm long cord, the
deviation for the rostral-caudal conus movement was found to strain would likely be smaller, foreseeably 1% or less, thus
be 6.4  4.1 mm within an overall range of 1.111.4 mm. The resulting in little relative motion between the HSCMS
fractional variations in these findings (standard deviation/ electrodes and the spinal cord. A large animal (ovine)
4 S. Viljoen et al. J Med Eng Technol, 2014; 38(1): 14

in vivo trial is now underway to investigate chronic discussions and technical assistance. We also thank R.
interactions between the HSCMS and the spinal cord surface Shurig and colleagues of Evergreen Medical Technologies
and histologic examination of explanted samples for evidence LLC for skillful fabrication of the prototype HSCMS devices
of tissue damage will be carried out. (The preliminary data and for the illustration used in Figure 1. AMS subject
from an earlier acute (non-survival) ovine in vivo study [3] classification: 92C10; 92C.
showed no evidence of tissue disruption.)
Lastly, from a HSCMS design perspective, it is now clear
Declaration of interest
that the lead loops of the devices implanted in some patients
must be sufficiently large to permit a total rostral-caudal range Authors Viljoen, Dalm, Reddy, Gillies and Howard may
of motion of up to 2 cm for the cord/membrane relative to the receive patent royalties from any commercial licensing of the
Oya Strap fixation point, i.e. 1 cm rostral and 1 cm caudal from HSCMS intellectual properties that might be negotiated by
the neutral position. HSCMS prototypes with loop area their respective institutions.
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