Normal MRI Appearance and Motion-Related Phenomena of CSF

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1 Lisanti et al. MRI of CSF MR Imaging Pictorial Essay Christopher Lisanti 1 Carrie Carlin 1 Kevin P. anks 2 David Wang 3 Lisanti C, Carlin C, anks KP, Wang D Keywords: CNS, CSF, MRI DOI: /JR Received January 4, 2005; accepted after revision June 7, The opinions and assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the Department of the rmy, the Department of the ir Force, or the Department of Defense. 1 Department of Radiology, Wilford Hall Medical Center, Lackland F, TX. 2 Department of Radiology, Fort Sam Houston, MCHE-DR, 3851 Roger rooke Dr., Fort Sam Houston, TX ddress correspondence to K. P. anks (kevin.banks@amedd.army.mil). 3 Department of Radiology, University of Colorado Health Sciences Center, Denver, CO. JR 2007; 188: X/07/ merican Roentgen Ray Society Normal MRI ppearance and Motion-Related Phenomena of CSF OJECTIVE. The purpose of this article is to review the normal appearance of CSF, flow physics in relation to CSF flow dynamics, and commonly encountered appearances and artifacts of CSF due to superimposed flow effects. CONCLUSION. Normal CSF has inherent MRI properties of low signal intensity on T1-weighted sequences and high signal intensity on T2-weighted sequences. However, the normal CSF signal is frequently altered by superimposed flow phenomena that can confound interpretation. ormal CSF has long T1 and long T2 N times that manifest as dark signal on T1-weighted images and bright signal on T2-weighted images. FLIR imaging results in nulling and dark CSF signal. The normal CSF signal is frequently altered by superimposed flow phenomena that can confound interpretation [1]. This article will review commonly encountered appearances and artifacts of CSF due to flow effects. CSF Physiology and Flow Dynamics The brain and spinal cord have a total volume of about 140 ml of CSF. Superimposed on this is an average of 500 ml per day production of CSF, with a net CSF flow from the lateral and third ventricles, through the cerebral aqueduct, out the fourth ventricle, and into the CSF-filled spaces of the spinal cord and cerebral convexities [2]. This simplification, however, does not take into account the pulsatile toand-fro movement of CSF due to the expansion and contraction of the brain produced by the expansion and contraction of the intracranial vessels associated with the cardiac cycle [3]. This pumping can result in CSF flow in the upper cervical spine that is approximately 40% as fast as the flow rate seen in the internal carotid arteries [3]. This results in significant motion-related effects that can alter the visualized signal of the CSF [1, 2, 4]. CSF Flow-Related Effects CSF flow-related phenomena can be divided into two categories: time-of-flight (TOF) effects and turbulent flow. TOF effects are further divided into TOF loss resulting in dark CSF signal and flow-related enhancement (FRE) producing bright CSF signal. Like TOF loss, turbulent CSF flow results in abnormally dark signal intensity. TOF Effects TOF Loss Signal formation in MRI depends on mobile protons experiencing the initial radiofrequency pulse and the subsequent refocusing mechanism. TOF loss typically occurs in spin-echo or fast spin-echo imaging when protons do not experience both the initial radiofrequency pulse and the subsequent radiofrequency refocusing pulse. TOF effects are more pronounced (darker signal) with faster proton velocity, thinner slices, longer TE, and an imaging plane perpendicular to flow (Figs. 1 and 2). In addition, TOF loss in single-shot fast spin-echo (SSFSE) techniques is related to whether the pulse sequence was acquired during systole with TOF loss or diastole without TOF loss (Fig. 3). Finally, gradient-recalled echo (GRE) techniques are resistant to TOF loss because of the short TE (Fig. 4). Typical locations for TOF losses include the lateral ventricles just superior to the foramen of Monro (Fig. 2), the third ventricle (Fig. 5), the fourth ventricle, and within the cervical and thoracic spinal canal [3, 5] (Fig. 3). Given the positive relationship between CSF velocity and TOF losses, this effect is magnified in individuals with an underlying abnormally hyperdynamic state such as hydrocephalus [2, 6]. In addition, laminar flow results in peripherally located protons 716 JR:188, March 2007

2 MRI of CSF moving at a slower velocity and leads to a reduction in TOF losses (Fig. 5). Techniques to minimize TOF losses include using a short TE technique such as true fast imaging with steady-state precession (true FISP) (Fig. 6), imaging parallel to flow, or thicker slices. FRE FRE or entry-slice phenomenon results in bright signal from unsaturated protons flowing into a slice replacing outflowing partially saturated protons during the TR. The unsaturated protons have their full longitudinal magnetization, which is flipped into the transverse plane by the initial radiofrequency pulse producing a higher signal than would be expected if they were stationary, partially saturated protons. Scanned sequentially, the first slices of the imaging volume into which the unsaturated protons flow show this effect most prominently, hence the term entry-slice phenomenon. FRE can be seen on T1- and T2-weighted images and is seen on more slices with singleslice acquisition techniques in which every slice is an entry slice (Fig. 7). These are most commonly seen on HSTE or SSFSE and in some GRE examinations. FRE can be reduced by applying saturation bands or by using ultrafast techniques such as true FISP (Fig. 8). FRE in FLIR imaging represents a special case in which the FRE is not due to unsaturated protons entering the imaging volume but due to partially saturated protons that do not experience the 180 inversion-recovery pulse. This results in a lack of nulling of the CSF and the subsequent appearance of the intrinsic bright T2 signal. The same locations that are common for TOF losses are also the most common for FLIR FRE (Figs. 9 and 10). There are certainly some TOF losses in this phenomenon; however, FRE usually dominates because the inversion time (TI) is much greater than the TE (2,200 vs 165 milliseconds), allowing more time for the protons to move during the TI than during the TE. These effects are most profoundly seen in patients with increased CSF volumes or flow dynamics (Figs. 11 and 12). Troubleshooting Techniques Either TOF loss or FRE can result in interpretive difficulties, and although most effects are seen in the axial plane, coronal (Fig. 7) and sagittal (Fig. 10) flow effects are also seen. Cross-referencing other imaging planes is helpful and comparing with faster imaging sequences such as GRE or true FISP imaging that reduce superimposed flow phenomena (Figs. 4 and 6). In addition, ghosting artifacts in the phase-encoding direction often accompany TOF- and FRE-related signal changes and can help point out the true nature of those changes. Turbulent Flow Turbulent flow results in a broader spectrum of proton velocities and a wide range of flow directions that are not seen in typical laminar flow. The varied flow velocities and directions result in more rapid dephasing and signal loss termed intravoxel dephasing. commonly encountered CSF flow artifact is the signal void in the dorsal subarachnoid space on sagittal T2-weighted images of the thoracic spine (Fig. 13). This artifact is due to a combination of the respiratory and cardiacrelated pulsatile CSF flow superimposed on cranially directed bulk CSF flow and turbulent flow from CSF moving from the ventral subarachnoid space to the dorsal subarachnoid space. This complex CSF motion results in phase incoherence leading to signal loss. Turbulent flow is often seen in the aqueduct of Sylvius (Fig. 14), the fourth ventricle, and some disease states (Fig. 15) and is sometimes seen from transmitted motion from arteries (Fig. 16). Turbulence dephasing can be reduced by shorter TE sequences and smaller voxel volume (decreased slice thickness or higher matrix). CSF Motion rtifacts The most common source of artifact in MRI is motion of the subject. Whereas random movement leads to blurring, periodic motion, such as with CSF pulsation, cardiac motion, and respiratory motion, leads to ghosting artifact. This occurs along the phaseencoding direction because phase information is acquired over an entire scan (minutes), whereas frequency information is acquired over a single frequency readout (milliseconds). Ghosting artifacts become more conspicuous as the source of the ghost becomes brighter relative to the surrounding tissues (Fig. 17). Ghosts can either be bright if they are in phase or dark if they are out of phase with the background signal [7] (Fig. 18). The number of ghosts varies inversely to the pulsation rate of the source. Troubleshooting Strategies to reduce CSF ghosting artifact include all the techniques for reducing TOF and FRE effects and increasing the number of excitations (but this results in longer scanning times). Identifying an identical ghost outside the body is useful in confirming ghosting artifact (Fig. 19), and swapping the phase and frequency encoding directions will change the axis of the artifact, rendering it less troublesome. Conclusion The interpretation of CSF and related abnormalities on MR images can be difficult because of the ever-present motion that is intrinsic to CSF. n understanding of the common flow-related appearances and locations, coupled with troubleshooting techniques, is critical to discerning flow effects from true abnormalities. dditional ghosting artifacts from the CSF can also mimic abnormality outside the CSF. References 1. Enzmann DR, Rubin J, DeLaPaz R, Wright. Cerebrospinal fluid pulsation: benefits and pitfalls in MR imaging. Radiology 1986; 161: radley WG, Kortman KE, urgoyne. Flowing cerebrospinal fluid in normal and hydrocephalic states: appearance on MR images. Radiology 1986; 159: aledent O, Henry-Feugeas MC, Idy-Peretti I. Cerebrospinal fluid dynamics and relation with blood flow: a magnetic resonance study with semiautomated cerebrospinal fluid segmentation. Invest Radiol 2001; 36: Kallmes DF, Hui FK, Mugler JP. Suppression of cerebrospinal fluid and blood flow artifacts in FLIR MR imaging with a single-slab three-dimensional pulse sequence: initial experience. Radiology 2001; 221: akshi R, Caruthers SD, Janardhan V, Wasay M. Intraventricular CSF pulsation artifact on fast fluid-attenuated inversion-recovery MR images: analysis of 100 consecutive normal studies. m J Neuroradiol 2000; 21: Parkkola RK, Komu ME, arimaa TM, lanen MS, Thomsen C. Cerebrospinal fluid flow in children with normal and dilated ventricles studied by MR imaging. cta Radiol 2001; 42: Wood ML, Runge VM, Henkelman RM. Overcoming motion in abdominal MR imaging. JR 1988; 150: JR:188, March

3 Lisanti et al. C Fig. 1 Schematic representation of factors involving occurrence and degree of time-of-flight (TOF) losses., Portion of excited mobile protons within CSF move out of slice volume between 90 and 180 pulse applications (TE/2). Only those protons subjected to both pulses will yield signal., More mobile protons move out of slice volume between 90 and 180 pulses as CSF flow velocity increases, which results in increasing TOF losses. Same effect occurs with increasing TE because mobile protons have more time to move out of slice volume before application of 180 refocusing pulse. C, Decreasing CSF flow angle relative to imaging plane results in lower effective velocity relative to slice volume, which results in decreasing TOF losses. V effective = effective velocity, V actual = actual velocity, COS = cosine. D, With increasing slice thickness, fewer mobile protons move out of slice volume between 90 and 180 pulses, which results in decreased TOF signal loss. D 718 JR:188, March 2007

4 MRI of CSF Fig. 2 Healthy 26-year-old female volunteer. xial T2-weighted image through level of lateral ventricles shows two foci of decreased CSF signal just superior to foramen of Monro (arrows) secondary to time-of flight losses. Fig year-old woman with hepatitis and pancreatitis undergoing MR cholangiopancreatography., T2-weighted single-shot fast spin-echo image acquired during systole shows time-of-flight signal losses (arrows) in ventral and lateral subarachnoid space., Same sequence acquired during diastole shows normal bright CSF signal surrounding thoracic spinal cord. JR:188, March

5 Lisanti et al. Fig year-old man with cervical spine pain after fall., xial T2-weighted image through cervical canal shows foci of signal loss in subarachnoid space (arrows) due to to-and-fro motion of CSF and associated time-of-flight (TOF) losses., Gradient-recalled echo T2* image at same level shows uniform CSF signal without TOF loss. Fig month-old male infant with seizures and developmental delay. xial T2-weighted image through third ventricle shows darker signal centrally (arrow) and brighter signal peripherally (arrowheads). This is common appearance of CSF in this region due to laminar flow effects. Laminar flow results in slower flow peripherally (less time-of-flight [TOF] loss) and faster flow centrally (more TOF loss). Fig year-old man with left sensorineural hearing loss., xial T2-weighted image at cerebellopontine angle shows signal loss anterior to basilar artery (arrows) due to time-of-flight losses., True fast imaging with steady-state precession at level of cerebellopontine angle shows uniform CSF signal. 720 JR:188, March 2007

6 MRI of CSF Fig year-old man with vertigo. Coronal postgadolinium T1-weighted image through third ventricle shows bright CSF signal (arrow) due to flowrelated enhancement (FRE) on entry slice. FRE rapidly diminished on deeper coronal slices (not shown.) Fig. 9 Healthy subject. xial FLIR image through level of lateral ventricles illustrates high signal (arrows) seen in lateral ventricles just superior to foramen of Monro due to flow-related enhancement. Fig. 8 Healthy subject., xial T2-weighted image through upper cervical spine shows multiple areas of abnormal bright CSF signal within periphery of subarachnoid space (arrows) due to flow-related enhancement, No saturation band was applied., xial T1-weighted image shows marked decrease in intensity of multiple foci of bright signal (arrows) in CSF due to application of superiorly placed saturation band. TR and TE remained unchanged. Fig year-old woman with headaches. Midline sagittal FLIR image shows flow-related enhancement (arrow) at foramen magnum initially thought to be Chiari I malformation. Sagittal T1-weighted images (not shown) showed normal dark CSF signal at foramen magnum. JR:188, March

7 Lisanti et al. Fig year-old man with remote history of left cerebellar astrocytoma resection., xial FLIR image shows significant flow-related enhancement (FRE) (arrow) in fourth ventricle., xial T2-weighted image shows time-of-flight (TOF) loss (arrow) in exact location of FRE in. This example nicely shows importance of background signal and sequence type on whether moving CSF protons will result in bright signal (FRE) or dark signal (TOF loss). Fig year-old girl with history of right frontal lobe glioma resection., xial FLIR image at level of lateral ventricles shows marked bright signal (arrows) secondary to flowrelated enhancement (FRE) in enlarged right lateral ventricle and surgical defect with minimal FRE in normal-sized left lateral ventricle., xial T1 postgadolinium image shows subtle FRE changes (arrow) in CSF in right lateral ventricle. 722 JR:188, March 2007

8 MRI of CSF Fig year-old man with thoracic spine pain. Sagittal T2-weighted image through thoracic spine shows globular signal loss in dorsal subarachnoid space (arrows) resulting from turbulence and time-of-flight effects associated with complex CSF flow. Fig year-old man with normal pressure hydrocephalus. Midline sagittal 3D fast spin-echo T2-weighted image shows significant loss of signal associated with increased velocities and turbulent flow in superior aspect of fourth ventricle (arrows). Corresponding sagittal T1-weighted image (not shown) shows normal dark CSF signal. Fig year-old woman with butterfly vertebral body and scoliosis., xial T2-weighted image at level of thoracic cord shows significant asymmetric time-of-flight signal losses in CSF (arrows)., Corresponding coronal T1-weighted image shows scoliosis and vertebral abnormalities. JR:188, March

9 Lisanti et al. Fig. 16 Healthy 32-year-old man. xial T2-weighted image through cerebellum shows focus of near-complete signal loss adjacent to basilar artery (arrow) from transmitted turbulence from artery and some time-of-flight (TOF) losses resulting in appearance of artifactual basilar aneurysm. Notice also mild TOF losses in CSF (arrowheads). Fig. 17 Healthy 2-year-old boy., xial FLIR image through craniocervical junction shows mild ghosting of spinal canal in phase-encoding direction., xial T2-weighted image at same level shows more conspicuous ghosting (arrow) due to increased brightness of ghosting source. 724 JR:188, March 2007

10 MRI of CSF Fig. 18 Healthy 2-year-old boy. s TE increases, ghosting artifact becomes more conspicuous due to increased brightness of ghosting source., xial proton-density-weighted image (TR/TE, 3,000/30) shows dark and bright ghosting (arrows) due to CSF flow within fourth ventricle., y increasing TE to 120 milliseconds, image shows dark and bright ghosting (arrows) become more evident. Fig year-old woman. xial fast spin-echo T2 image shows bright ringshaped lesion (black arrows) in left lobe of liver due to ghosting of CSF motion. Notice faint ring ghost more posteriorly and more conspicuous ghost posterior to patient (white arrow). Ghosts and spinal canal are all in anteroposterior phase-encoding direction, which confirms identity of this lesion as ghosting artifact. JR:188, March