In this article, we illustrate the main advanced magnetic resonance imaging (MRI) techniques used for imaging of the spine and spinal cord in children and adults. This work focuses on daily clinical practice and aims to address the most common questions and needs of radiologists. We will also provide tips to solve common problems with which we were confronted. The main clinical indications for each MR technique, possible pitfalls and the challenges faced in spine imaging because of anatomical and physical constraints will be discussed. The major advanced MRI techniques dealt with in this article are CSF, (cerebrosopinal fluid) flow, diffusion, diffusion tensor imaging (DTI), MRA, dynamic contrast-enhanced T1-weighted perfusion, MR angiography, susceptibility-weighted imaging (SWI), functional imaging (fMRI) and spectroscopy. Teaching Points � DWI is essential to diagnose cord ischaemia in the acute stage. � MRA is useful to guide surgical planning or endovascular embolisation of AVMs. � Three Tesla is superior to 1.5 T for spine MR angiography and spectroscopy. � Advanced sequences should only be used together with conventional morphological sequences. . . . . Keywords Spinal cord Perfusion Spectroscopy Magnetic resonance angiography Diffusion tensor imaging Introduction These techniques are feasible at 1.5 and 3 T with a clear advantage of 3 T for magnetic resonance angiography (MRA) Advanced MRI techniques applied to the spinal cord have and spectroscopy. remained difficult to put into practice until recently. Until Characterisation of intramedullary lesions is challenging now, advanced imaging techniques of the spine have relied with conventional sequences, and, on numerous occasions, it on significant contributions from MR physicists to apply them is difficult to identify the origin of the lesion, distinguish be- to clinical routine. tween inflammation and ischaemia, and correctly date an isch- aemic lesion as acute or hyperacute. Conversely, advanced sequences allow a much better depiction of the anatomy, such as diffusion tensor imaging (DTI) for pre-surgical planning of spinal tumours or MRA to accurately localise the shunt and * M. I. Vargas nidus of an AVM. firstname.lastname@example.org In this article, we illustrate the main advanced techniques, such as cerebrospinal fluid (CSF) flow, diffusion and diffusion Division of Neuroradiology, DISIM, Geneva University Hospitals tensor imaging (DTI), dynamic magnetic resonance and Faculty of Medicine, Rue Gabrielle-Perret-Gentil 4, 1211, Geneva 14, Switzerland angiograpy (MRA), dynamic contrast-enhanced T1-weighted perfusion, susceptibility-weighted imaging (SWI), functional Division of Radiology, DISIM, Geneva University Hospitals, Geneva, Switzerland imaging and spectroscopy. The main technical challenges faced in spine imaging and the clinical applications of these Division of Neuroradiology, Strasbourg University Hospitals, Strasbourg, France techniques in children and adults are also discussed. 550 Insights Imaging (2018) 9:549–557 Advantages and disadvantages of high field the phase encoding gradient is applied in the slice encoding strength direction. These phase-contrast sequences require ECG trig- gering since the blood and CSF flow velocities vary during the The use of high field strength on MRI in brain imaging has cardiac cycle. allowed an increased signal-to-noise ratio (SNR) and de- Flow measurement is performed in the sagittal plane to creased acquisition time. However, the situation is not the visualise in-plane CSF flow. In this case, care has to be taken same with advanced sequences in spine and spinal cord imag- if the phase encoding direction is chosen since cardiac and ing. The main challenges faced in spine imaging relate to the respiratory motion are highly deleterious to image quality small dimensions of the spinal cord (approximately 12 to and flow quantification. 14 mm in diameter), inhomogeneity of B0 on T1 imaging, The velocity encoding gradient in the sequence should artefacts due to the CSF flow, which are more significant on be set between 10 and 20 cm/s and be increased if aliasing the dorsal spine, and also artefacts due to breathing, patient artefacts are observed. Bunck et al. reported10cm/sin motion and swallowing . Magnetic susceptibility artefacts volunteers and 20 cm/s in patients where a specific pathol- are also important because of interfaces between different ogy could lead to increased velocity due to narrowing of structures such as bone, lungs and fat. the CSF canal. Sometimes, high field strength may be a limitation be- Flow can be measured directly in the three spatial direc- cause of the greater effect of susceptibility artefacts (going tions to improve sensitivity to both the in- and through-plane linearly with the field strength). The distortions of the im- velocities and also to determine the flow direction. This se- ages are thus important particularly in the spine where the quence, which provides data in a 3D volume, is promising but proximity with the lungs creates high susceptibility arte- has the disadvantage of long acquisition times (12–14 min facts. On the other hand, high field strength in the DTI of versus 3–5 min for the 2D sequence ). the cervical spine causes geometric distortion. This has been partially solved by the new sequence types [readout segmentation of long variable echo train (RESOLVE) Three-dimensional MR T2 high resolution available on Siemens systems or zoomed EPI available on all systems, for example]. Three-dimensional MR T2 high resolution is an isotropic se- For other sequences such as CSF flow and perfusion imag- quence also known as the 3D CISS (constructive interference ing, 1.5- or 3-T MR can be used with the same final result. in steady state), 3D True-FISP (fast imaging with steady-state Additionally, high field strength offers a real added value for precession) or FIESTA (fast imaging employing steady-state MRA and spectroscopy; it produces higher SNRs and faster acquisition) sequence (Fig. 2). acquisition minimising motion artefacts. This sequence allows good depiction of smaller structures because of high spatial resolution, high T2 contrast and its isotropic properties, which permit visualisation in three planes Advanced sequences without distortion. The main clinical indications are: CSF flow – thin septa in post-traumatic cysts The application of this sequence in spinal cord imaging is for – walls of arachnoid cysts or arachnoid webs (Figs. 1 and 2) depicting cystic lesions, such as arachnoid or leptomeningeal – inner structure of cystic tumours cysts (Fig. 1), the latter often resulting from haematomas after – normal and dilated vessels on the surface of the spinal trauma, which breakdown into haemosiderin and its deriva- cord in dural fistulas and AVMs tives and may cause arachnoiditis [2, 3]. CSF flow techniques – post-traumatic pseudomeningoceles are usually coupled with T2 high-resolution sequences, which – dural breach and CSF leak in hypotension of CSF serve the double purpose of helping to better depict lesions – Tarlov cysts and also to generate an anatomical mask. Phase contrast MRI is a unique approach to measuring flow A larger FOV can be obtained in the coronal and sagittal in vivo. It relies on the principle that motion in a voxel induces planes, but axial images are also possible. additional dephasing of the signal. With an appropriate se- Other 3D T2 sequences such as space, CUBE or VISTA, quence providing phase images in addition to magnitude im- which are spin echo sequences, are less sensitive to flow ages, it is possible to measure the flow velocity in a voxel . and susceptibility artefacts , allowing clear depiction of A phase encoding gradient can be applied in one of the three the nerve root sheaths. The most common pitfall of these directions of space to detect flow in that specific direction. If sequences is the Gibbs artefact mimicking superficial the flow going through the imaging plane needs to measured, siderosis (Fig. 3). Insights Imaging (2018) 9:549–557 551 Fig. 1 Sagittal (a)and axial (b) T2WI shows hyperintensity of the cord (arrow), which is deformed (scalpel sign), suggesting an arachnoid web. Sagittal 3D T2WI (b) better demonstrates the web (arrow). Sagittal flow sequences (d,e) show decreased CSF flow posteriorly to the cord due to the arachnoid web Dynamic MRA thrombus in the vessel lumen, particularly in a small artery such as the AKA. On the other hand, dynamic MRA can be Clinical applications include investigation of vascular very useful in showing a dissection or a partially malformations such as dural fistulas (Fig. 4) and arteriove- thrombosed aneurysm of the aorta. However, it plays no nous malformations and identification of the exact location role in the workup of cavernomas as they are angiograph- of the artery of Adamkiewicz (AKA) for presurgical plan- ically silent. CT is an excellent technique for imaging of ning for tumours to facilitate endovascular treatment. In large vessels, but it does not allow visualisation of spinal case of ischaemia, it is very difficult to visualise the cord ischaemia. Fig. 2 CT scan (a,b,c)performed in a 61-year-old females complaining of back pain after a fall shows several paraspinal lesions (arrows), which are difficult to characterise by this technique. A CISS MR sequence (d) clearly shows these to be extradural cysts. Note that there is no enhancement on T1 FS Gd (e,f,g) 552 Insights Imaging (2018) 9:549–557 Fig. 3 FSE T2 shows an enlarged ependymal canal at the C5 level (white arrow in a). Note that the same abnormality appears larger on the SPACE T2 sequence and also the false image of superficial siderosis on the cervical spinal cord (black arrows in b) Fig. 4 Sagittal T2WI (a) demonstrates multiple dilated vessels with corkscrew appearance surrounding the spinal cord (a); 3D MRA reformat nicely illustrates the arteriovenous shunt at the level of T6 on the right (arrow in b) confirmed by DSA (c) Insights Imaging (2018) 9:549–557 553 The main challenges of dynamic MRA are the small size of 18] because of the lower intracellular water content. This is vascular structures in the spine and the dynamic aspect of this the main reason why b500 or b900 is used in spinal imaging sequence. These are also the main reasons why high field and not b1000. strength is useful because of its higher SNR. DWI and DTI are challenging techniques in spinal imaging There are two techniques for performing dynamic MRA: for several reasons, including the small size of the cord rela- dynamic sequences with a temporal resolution of approxi- tive to the brain and respiratory and cardiac motion artefacts. mately 1 min (3 phases: arterial, venous and delayed, and an Therefore, spine diffusion imaging requires high spatial reso- additional later acquisition at high spatial resolution) and lution, which should be combined with distortion reduction 4D imaging . techniques and homogeneous fat saturation. These goals are The first relies on a 3D gradient echo T1-weighted se- difficult to achieve with the broadly used single-shot spin echo quence with a field of view comprising the descending aorta EPI diffusion sequence, especially when image acquisition is as well as the spine in the sagittal plane. The angiography in the sagittal plane, which is preferred for the evaluation of technique uses a noncontrast image that is subsequently the spine. Specific aspects are (1) fat saturation, (2) imaging subtracted from the arterial phase image. An important aspect distortion and (3) b-values and directions. is the timing of the imaging. The arterial bolus remains in the arteries for a short period of time; thus, imaging should be (1) Conventional fat saturation with spectral selection of the done at a precise time to eliminate venous contamination. fat peak based on CHESS (chemical shift selective) has This timing depends on the injection rate and also on the the advantage of being fast but often delivers poor results cardiovascular status of the patient. in spine imaging. In dorsal areas, an inversion recovery The utilisation of blood pool agents or doubly concentrated technique, such as STIR (short tau inversion recovery), is contrast media may nevertheless facilitate image acquisition more robust in eliminating the signal from fat and im- and subsequent analysis. proving image quality. However, this causes a reduction The other technique for MRA relies on a 4D sequence also in the signal due to the inversion pulse. A compromise is known as time-resolved angiography with stochastic trajecto- to use SPAIR (spectral attenuated inversion recovery) ries (TWIST)  or 4D time-resolved MR angiography with a preparation, which shows relatively robust saturation keyhole (4D-TRAK) with a spatial resolution of 1 mm and provided the shim box is placed correctly in the area of temporal resolution of approximately 1.3 s. interest avoiding the lungs. Diffusion and diffusion tensor imaging A recently available method to suppress the fat signal is the Dixon technique . It relies on the principle that water and fat do not precess at the exact same frequency and that they Acute ischaemia is one of the main clinical indications for DWI, is seen as high signal on trace images and decreased ADC can be either in or out of phase after the preselected time to without enhancement (Fig. 5), which only appears in the sub- echo. This technique provides very homogeneous fat- acute phase . The main causes in adults are atherosclerosis, saturated images on large fields of view. cardiac surgery and minimally invasive procedures, compres- sion of the radicular artery by a disc and minortraumato (2) Diffusion imaging uses a single-shot EPI sequence. the cervical spine in the setting of degenerative changes. Throughout the long echo train, phase errors will ac- In children, minor trauma is a cause of ischaemia related to cumulate, resulting in spatial mismatch in the recon- fibrocartilage emboli  (Fig. 5) and also arterial spasm. structed image. The longer the echo train and the Other causes include traction for scoliosis after orthopaedic higher the resolution, the more pronounced the distor- surgery , complications of cardiac surgery, sickle cell tions will be. Distortions will also be enhanced be- anaemia and umbilical artery catheter in the neonate. cause of susceptibility differences between different DWI is also used to differentiate between spondylodiscitis spinal tissues (bone, intervertebral discs, cerebrospi- and inflammatory degenerative changes . FA and ADC nal fluid, etc.). values may be used to predict gain of function in patients with cervical spondylotic myelopathy after decompressive surgery Reducing the readout bandwidth minimises this distortion. . To achieve this, parallel imaging can be used together with a DTI tractography is used for pre-surgical planning of rectangular field of view. Another option is to choose a trans- tumours (Fig. 6) as the generated cartography is the verse orientation with an isotropic voxel resolution. Another only method allowing the neurosurgeon to visualise the alternative to this problem is segmentation of the EPI readout tracts in vivo . in either the phase or readout direction. A more detailed ex- Unlike in the brain, diffusion of water molecules in the planation of distortion reduction in spine diffusion imaging can be found in: [20–22]. spinal cord occurs mainly in the cranio-caudal direction [8, 554 Insights Imaging (2018) 9:549–557 Fig. 5 A 14-year-old male who suffered minor trauma. Spine MR performed 24 h later shows increased signal intensity on T2WI (a,d)(arrows) and DWI (e) reflecting ischaemia. Note an acute wedge fracture of T12 (*) (3) b = 500 s/mm is often chosen at 1.5 T since it produces a generate DTI parameters such as FA or MD is six, a more sufficient SNR to allow satisfactory interpretation of the reasonable value would be around 20. images without being too low, and thus too sensitive, to perfusion effects . This value can be increased at 3 T Dynamic contrast-enhanced T1-weighted perfusion because of the higher SNR. Dynamic contrast enhancement (DCE) is a technique that al- For DTI, the optimal number of diffusion directions varies lows dynamic visualisation of contrast behaviour in tissues. It depending on the authors , a higher number being often is the technique of choice to assess microvascularisation, in preferred. While the minimum number of directions to particular in the context of tumour growth, because it provides Fig. 6 Patient with multiple myeloma and several vertebral fractures, medullaris (b,c,f,g). On tractography (d,e), destruction of the fibers of treated by vertebroplasty. No enlargement or enhancement of the conus the conus medullaris can be seen; this translates into a secondary lesion medullaris is visible (a). Spine MR performed approximately 7 months with rapid growth later shows hyperintensity and nodular enhancement of the conus Insights Imaging (2018) 9:549–557 555 information about the tumour vasculature and the effects of Susceptibility weighted imaging (SWI) treatment (Fig. 7). This technique is used in brain imaging for tumour characterisation and for distinguishing between SWI is a sequence based on the magnetic susceptibility differ- radionecrosis and true tumour progression. In spine imaging, ences between tissues. Reconstructions of magnitude and DCEisusedtocharacterisetumours andtoevaluate phase images are possible. The acquisition of this sequence extradural spinal metastases and their vascularisation , does not need the administration of contrast medium. which in turn helps in the selection of patients amenable to SWI is principally used at the level of the brain to detect endovascular treatment. micro-haemorrhages, calcifications, iron and deoxy-Hb. The goal of DCE is to quantify tissue permeability with the Concerning the spine, few articles exist concerning the use use of specific models such as the Tofts model or equivalent of this sequence at 1.5 T. In our opinion, its use is possible . This two-compartment model provides physiologically but has not been extended to daily clinical practice because of relevant parameters such as the K [volume transfer con- limitations in spatial resolution and multiple artefacts due to trans stant between blood plasma and extravascular extracellular phase-encoding directions, bone-tissue interfaces, flow and space (EES)], K (rate constant between EES and blood plas- increased noise. This sequence is particularly sensitive to sub- ep ma) and V (volume of EES per unit volume of tissue, i.e., the tle changes of the local magnetic susceptibility variances, de- volume fraction of the EES). creased signal-to-noise ratios, etc. . To generate these parameters, imaging should be per- The possibly clinical indications are visualisation of normal formed at relatively high temporal resolution (between 2 to venous anatomy , identification of haemorrhage, evalua- 15 s) and over 5 to 10 min post administration of contrast tion of the efficiency of treatment of spinal arteriovenous media. Using a 3D-T1 spoiled gradient recalled echo sequence malformations and evaluation of changes in venous oxygena- to dynamically image the contrast arrival and washout is rec- tion  with SW phase imaging. ommended . This sequence is very sensitive to T1 varia- tions and is fast enough to produce a suitable temporal reso- Spectroscopy lution while maintaining a sufficient SNR. For the modelling, it is necessary to convert the signal intensity curve into a Gd Spectroscopy shows the concentration of normal metabolites concentration curve, which can only be done with knowledge in a specific anatomic location and changes in those metabo- of the T1 values before contrast injection. Usually, the two flip lites in case of pathology. Few works have shown the feasi- angle method is chosen because it is fast and reliable. This bility of spectroscopy in spinal cord imaging. Spectroscopy technique has been more widely used in the brain but has also has, nevertheless, been used to characterise and differenti- shown promising results in spine imaging, such as preclinical ate tumours  from inflammatory pathologies, in amyo- research in spinal cord injury assessment [28, 29]. trophic lateral sclerosis or in the follow-up of cervical Fig. 7 A patient with spinal cord glioblastoma. a Sagittal T1 post- curve) in the mass but also in the posterior paraspinal soft tissues gadolinium MR image shows an enhancing intramedullary mass. b reflecting contrast extravasation due to postoperative changes. This case Corrected Vp (volumetric plasma volume) parameter of T1 perfusion is illustrates that T1 perfusion, particularly corrected Vp, allows detection of increased in the mass. c and d Increased K and AUC (area under the true tumour hypervascularisation trans 556 Insights Imaging (2018) 9:549–557 creativecommons.org/licenses/by/4.0/), which permits unrestricted use, spondylotic myelopathy . Furthermore, Holly et al. distribution, and reproduction in any medium, provided you give appro-  showed that spectroscopy may be of value in priate credit to the original author(s) and the source, provide a link to the predicting neurological outcome in patients with cervical Creative Commons license, and indicate if changes were made. spondylotic myelopathy after surgery. Spectroscopy of the spinal cord presents a real challenge because of the small dimensions of the cord, flow artefacts, motion artefacts during the cardiac and respiratory cycles, the References deep anatomical location  and B0 inhomogeneity, which is particularly deleterious to spectroscopy of the spine. For this 1. Vargas MI, Delavelle J, Kohler R, Becker CD, Lovblad K (2009) reason, B0 shimming is essential. Saturation bands and pulse Brain and spine MRI artifacts at 3Tesla. J Neuroradiol 36:74–81 2. Caremel R, Hamel O, Gerardin E et al (2013) Post-traumatic syrin- triggering  are used to reduce CSF flow artefacts. gomyelia: what should know the urologist? Prog Urol 23:8–14 The sequence used is PRESS (point-resolved spectrosco- 3. Fehlings MG, Austin JW (2011) Posttraumatic syringomyelia. J py), which produces better results with a long TE of around Neurosurg Spine 14:570–572 discussion 572 135 or 280 ms than with short TE below 40 ms. Currently, this 4. 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