1991, The British Journal of Radiology, 64, 89-97
VOLUME 64 NUMBER 758
FEBRUARY 1991
The British Journal of Radiology Observation of cerebrospinal fluid flow with echo-planar magnetic resonance imaging By M. K. Stehling, MD, PhD, *J. L Firth, FRCS, tB. S. Worthington, BSc, D. N. Guilfoyle, PhD, R. J. Ordidge, PhD, R. Coxon, PhD, A. M. Blamire, BSc, P. Gibbs, BSc, *P. Bullock, FRCS and P. Mansfield, PhD, FRS Department of Physics, University of Nottingham and Departments of 'Neurosurgery and tAcademic Radiology, Queen's Medical Centre, Nottingham NG7 2RD, UK (Received April 1990 and in revised form August 1990) Keywords: Echo-planar magnetic resonance imaging, Cerebrospinal fluid
Abstract. Using echo-planar (EP) magnetic resonance imaging (MRI), cerebrospinal fluid (CSF) flow patterns have been demonstrated in the normal subject and patients with pathological conditions including communicating hydrocephalus, aqueduct stenosis and syringohydromyelia. Snap-shot imaging times of 128 ms allow detailed demonstration of transient intraventricular CSF flow patterns, which is not possible with conventional MRI. The potential of EPI as a method for qualitative and quantitative assessment of CSF dynamics is illustrated.
A number of different approaches have been made using conventional two-dimensional Fourier transform magnetic resonance imaging (2D-FT MRI) techniques to image cerebrospinal fluid flow within the ventricular system and basal cisterns (Bergstrand et al, 1985; Bradley et al, 1986; Jolesz et al, 1987). Superimposed on the slow overall circulation of cerebrospinal fluid (CSF) are respiratory and cardiac dependent pulsatile flow which can be identified on MR imaging by "time of flight" effects (Singer, 1978) as well as reversible and irreversible phase changes (Wehrli et al, 1984). Conventional MRI techniques, however, employ repetitive data acquisition over an extended period of time so that flow patterns can only be depicted as a weighted average over time. Even when time-resolved flow information has been obtained by means of cardiac gating, only regular and repetitive features of flow are captured and information about transient flow patterns is lost. The requirements for an ideal method of studying CSF flow in vivo would include the following: first, it should be non-invasive; secondly have no planar restrictions; thirdly be capable of gathering data very rapidly; and finally provide directional information and quantification of flow over the full range of values found in normal subjects and pathological conditions. Echo-planar imaging (EPI) is an ultrafast nuclear magnetic resonance technique able to produce snap-shot images in typically 30-100 ms (Mansfield, 1977). We have applied EPI operating in a real-time mode to Please address reprint requests to Professor P. Mansfield. Vol. 64, No. 758
observe CSF dynamics in the normal subject and several patients with pathological conditions including hydrocephalus and syringohydromyelia. The first observations of CSFflowby EPI and attempts to quantify slow flow have been reported previously (Mansfield et al, 1986; Howseman et al, 1987). The ability to depict CSF signal intensity changes with EPI allows demonstration of CSF flow phenomena with high spatial and temporal resolution. This allows a detailed description of individual flow patterns and their evolution in time. The simulation of flow phenomena in phantoms provides a basis for qualitative interpretation of the CSF flow patterns which are observed in vivo. Technique
Imaging was carried out on our home-built 0.52 Tesla EPI scanner. An actively shielded whole-body gradient coil system was used in conjunction with a purpose-built head-size birdcage RF coil. The pulse sequence and A>space diagrams in Fig. 1 show how an EP image is acquired. The rapidly switched frequency encoding j-gradient creates 128 gradient echoes in 128 ms. Each gradient echo corresponds to one of the 128 lines in A>space. Phase encoding is obtained through ^-gradient bursts (blips) at the ^-gradient zero-crossings. Full details of the modulus blipped echo-planar single shot technique (MBEST) as used for transaxial scanning is given elsewhere (Howseman et al, 1988; Ordidge et al, 1988; Stehling et al, 1989). For imaging in the coronal and sagittal planes, the 89
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Figure 1. MBEST and EPI (dashed) pulse sequence diagram (A) and fc-space trajectories (B). For coronal plane EPI, the rapidly switched frequency encoding gradient is along the >>-axis, while for sagittal EPI it is along the x-axis. The chemically selective phase (shaded) provides lipid/water proton signal suppression when required.
Figure 2. Six consecutive 64 ms MBEST snap-shots of circular flow in a 20 cm diameter water phantom. Dark areas indicate partially saturated spins (TR « 620 ms), moving within the image plane. In the first image of the sequence (TR = oo) flow, although present, is not detected. Bright areas are caused by flow components perpendicular to the image plane, resulting in flow related enhancement.
90
slice selective gradient is applied along the jc-axis and the j-axis respectively. The extent of the imaging plane along the z-axis is defined by the sensitive volume of the RF coil. This provides a reasonably sharp cut-off which avoids aliasing in the z-direction. Slice selection is followed by a standard EPI pulse sequence (Mansfield, 1977). This employs a non-blipped phase encoding gradient and creates the zig-zag fc-space trajectory shown dashed in Fig. IB. The constant low level phase encoding gradient was necessary in this case because the high inductance of the z-gradient coil prevented application of the z-gradient blips. All images are based on 128x128 pixel arrays with approximately 1.7 mm inplane resolution and a slice thickness of 10mm. Acquisition of a complete two-dimensional EP image takes 128 ms. For the creation of movie loops, triggered image acquisition was employed with 16 progessively delayed steps through the cardiac cycle triggered from a peripheral pulse monitor. The repetition time (TR) delay between consecutive frames was of the order of 2 s which allowed almost complete T, relaxation of brain tissue between shots. CSF proton spins were partially saturated and thus sensitized to flow through the imaging plane. Grey-white matter contrast in MBEST and EP images is based on the intrinsic T^-weighting of these techniques, caused by the delayed signal maximum of the echo-train (for full explanation see the following: Howseman et al, 1988; Ordidge et al, 1988; Stehling et al, 1989). To a first approximation the contrast in the MBEST images shown here is equivalent to that provided by a 3000/63 spin echo sequence. Results Flow phantoms
To verify the theoretical flow dependency of EPI two different phantoms were used to demonstrate the effects of bulk flow in EPI images. The British Journal of Radiology, February 1991
CSFflow shown by echo-planar MRI
Figure 3. Six 64 ms MBEST images demonstrating signal dephasing caused by turbulent in-plane flow. The flow patterns were induced by squirting 1 ml of water through a narrow nozzle into 150 ml of stagnant water.
Flow into the imaging plane was produced with the "swirling water" phantom. A simple cylindrical 20 cm diameter plastic bottle filled with tap water was spun about its longitudinal axis to establish circular flow and the contents of the bottle were then imaged. The eight 64 ms MBEST images shown in Fig. 2 were acquired with a TR of 620 ms between consecutive images. The maximum linear flow velocity at the perimeter of the bottle was approximately 30 cm/s. The high signal intensity spiral patterns in images 2-8 are caused by the introduction of fresh spins into the imaging plane by the component of flow perpendicular to it. These newly added spins provide an indication of the in-plane component of the flow. The absence of flow patterns in the first image, with flow already established but no preceding excitation, clearly indicates the Tx relaxation based nature of this phenomenon. Rapid in-plane flow was demonstrated with a phantom composed of two 150 ml plastic bottles connected by a 2 mm bore plastic tube. Approximately 1 ml of water was gently squeezed through the plastic tube from one bottle into the stagnant water of the bottle depicted in the images in Fig. 3. Images were obtained with incremental time delays after squeezing and show the development of a jet originating from the small nozzle at the end of the connecting tube. Turbulent flow within the jet causes spin dephasing and results in a signal void. Note the detailed patterns of turbulent flow in the upper part of the phantom. Vol. 64, No. 758
CSF flow A representative series of coronal images from a normal volunteer is shown in Fig. 4. These were taken through a single plane intersecting the cerebral hemispheres, brainstem and upper cervical cord. The CSF within the ventricular system, basal cisterns and subarachnoid pool around the cord appears bright. Sequential images triggered to the cardiac cycle show that in systole the signal form from the CSF at the foramen magnum disappears, indicating rapid CSF flow between the intracranial and intraspinal compartments. Pulsation of CSF within the cervical theca and basal cisterns is a phenomenon which was well known to neuroradiologists when carrying out Myodil myelography and cisternography (Du Boulay, 1966). This is strikingly displayed on the movie loop and with improvements in spatial resolution pulsatile movement of the brain parenchyma should be detectable. Evidence for vascular pulsation based brain motion has recently been demonstrated by MR velocity imaging (Feinberg & Mark, 1987). Complex flow patterns within the ventricles have been demonstrated in a patient with aqueduct stenosis. Figure 5 shows a movie loop of 16 coronal 128 ms acquisition time EP images 2 cm posterior to the foramina of Monro. Areas of high signal intensity are seen within the lateral ventricles which wax and wane. Peripheral to these are irregular bands of low signal intensity. The former represent flow perpendicular to the imaging 91
M. K. Stehling et al
Figure 4. Four snapshots from a 16 frame coronal EPI movie loop through the cerebrum and brainstem is shown. Signal void in the subarachnoid spaces at the foramen magnum is caused by rapid CSF flow. Vascular pulsation related brain movement is more obvious when the sequence is displayed as a movie loop. (Ref. 04503.)
plane, that is along the bodies of the ventricles, whereas the latter represent in-plane rapid flow, which is assumed to be secondary to the jet of CSF ejected through the foramina of Monro in systole. Eight frames from a transaxial 16 frame MBEST movie loop of the same patient are shown in Fig. 6 and again an area of signal attenuation is seen at the foramina of Monro during systole. As in the coronal movie loop, the flow pattern is more pronounced on the right side. These findings have been confirmed by preceding the MBEST sequence with a flow sensitizing sequence 92
(Ordidge et al, 1989) in order to obtain quantifiable flow information. The flow sensitizing gradient was applied in the z-direction, i.e. along the patient axis. The z-component of CSF flow is mapped in Fig. 7 for three different phases of the cardiac cycle. Figures 7A, 7B and 7C correspond approximately to Figs 6C, 6G and 6H respectively. For uniform flow velocity v within a pixel, the image signal intensity, /, is given by / oc sinfcv where k is a constant determined by the flow encoding sequence parameters. The flow map demonstrates general low level flow throughout the ventricles (blue), The British Journal of Radiology, February 1991
CSF flow shown by echo-planar MRI
Figure 5. Sixteen frame coronal EPI movie loop through the lateral and third ventricle, posterior to the foramen of Monro. The clock indicates the phase of the cardiac cycle with respect to the R wave, frame A. Flow along the body of the ventricles appears bright owing to flow related enhancement. Dark areas reflect rapid flow, originating at the foramen of Monro. (Ref. 04004.) and confirms the more rapid flow through the right foramen in systole (yellow and red). Note that the flow maximum is seen within the lateral ventricles. At the foramina, little signal is depicted, which may reflect turbulence resulting in loss of phase information. Figure 8 shows six coronal 128 ms acquisition time EP images in a patient with communicating hydrocephalus. The imaging plane intersects the lateral ventricles, aqueduct and fourth ventricle. During systole (frames A-C), a flame shaped area of signal void due to flow can be seen to originate from the aqueduct and extend into the upper part of the fourth ventricle. This confirms that the aqueduct is patent. The flow plume decays away in frames D - F during diastole. Figure 9 shows all 16 frames of a sagittal EPI movie loop in a patient with syringohydromyelia. Multiple areas of signal attenuation are seen in the fluid Vol. 64, No. 758
contained within the thin walls of the syrinx. These areas of signal loss indicate complex flow patterns within the fluid contained in the central cavity. Complex flow of CSF within syrinx cavities in five patients was also found by Le Bihan et al (1987), using the technique of mapping intravoxel incoherent motion.
Discussion Approximately 500 ml of CSF are secreted each day, largely by the choroid plexus within each lateral ventricle, and this circulates through the ventricular system and the cerebral and spinal subarachnoid systems before being absorbed by the arachnoid villi which are associated with the major dural venous sinuses. Superimposed on the slow background of circulation of CSF are respiratory and cardiac depen93
M. K. Stehling et al
Figure 6. Eight transaxial MBEST images at the foramina of Monro of the same case as in Fig. 5. Signal enhancement due to flow is demonstrated at the foramina in systole (frames G and H). (Ref. 04005.)
dent pulsatileflows.The mechanisms of CSF propulsion along these pathways are still incompletely understood. Cardiac dependent CSF motion occurs secondarily to cerebral perfusion. The existence of a third ventricular pump has been postulated (O'Connell, 1943) and much support for this hypothesis has been provided through observations made during pneumoencephalography (Du Boulay et al, 1972). In a recent study in normal individuals using gated high resolution MRI (Mark et al, 1987), the flow results were best explained by postulating a synchronous pulsatile flow of CSF at the foramen
of Monro and the aqueduct with an antegrade flow during systole and a retrograde but smaller flow during diastole, giving a net antegrade flow of CSF which enters the basal cisterns. The observation of pulsatile flow at the foramen of Monro suggests that the lateral ventricles do play a part in generating CSF flow, perhaps via expansion of the choroid plexus. Certainly considerable motion of CSF occurs within the lateral ventricles in pathological conditions, as we have observed in several cases in addition to the patient with aqueduct stenosis reported above.
Figure 7. Flow maps obtained at different phases of the cardiac cycle in the same patient as Figs 5 and 6: (A) diastole; (B) early systole; (C) mid-systole. Flow sensitization is along the z-axis or patients axis, i.e. in a direction perpendicular to the plane of the flow maps. Theflowvelocity is proportional to arcsin(T), where / is the signal intensity in the map (blue, low intensity; white, high intensity). Flow is more pronounced in the right foramina of Monro, in accordance with theflowpatterns in the standard MBEST images of Figs 5 and 6. (Ref. 04005.) 94
The British Journal of Radiology, February 1991
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Figure 9. Sixteen frames of a sagittal EPI movie loop, showing intracavitary fluid flow in a syringohydromyelia. Areas of signal void indicate turbulent flow in eddies, which travel caudally during systole. Note the development of a jet in systole at the narrowed part of the spinal canal (arrow). (Ref. 21301.)
CSF flow shown by echo-planar MRI Conclusion
We have shown that EPI can be used to study flow patterns in the CSF pathways with high spatial and temporal resolution. In the MBEST technique, both real and imaginary components of the NMR signal are collected, from which magnitude and phase information can be derived and this can be used to study transient, complex CSFflowpatterns in real time. Using aflowencoding sequence (Ordidge et al, 1989), we have produced coronal maps indicating CSFflowin the lateral ventricles of a patient with aqueduct stenosis. In these results localized flow is a direct and quantifiable function of localized signal intensity. Our results indicate that EPI is able to provide both qualitative and quantitative information in real-time. This could be of value for studying CSF flow dynamics in both normal and abnormal situations. Acknowledgments We thank the Medical Research Council, the Department of Health and the British Heart Foundation for their support of the echo-planar imaging programme. M.St. thanks the Deutsche Forschungsgemeinschaft for a stipend. We are grateful to Mark Symms for help with data processing and photography. References BERGSTRAND, G., BERGSTROM, M., NORDELL, B., STRAHLBERG, F., ERICSSON, A., HEMMINGSON, A., SOERKER, G., THUOMAS,
K. A. & JUNG, B., 1985. Cardiac gated MR imaging of cerebrospinal fluid flow. Journal of Computer Assisted Tomography, 9, 1003-1006. BRADLEY, W. G., KORTMAN, K. E. & BURGOYNE, B., 1986.
Flowing cerebrospinal fluid in normal and hydrocephalic states: appearance on MR images. Radiology, 159, 611-616. Du BOULAY, G. H., 1966. Pulsatile movements in the CSF pathways. British Journal of Radiology, 39, 255-262. Du BOULAY, G. H., O'CONNELL, J., CURRIE, J., BOSTICK, T. &
JOLESZ, F. A., PARZ, S., HAWKES, R. C. & LOPEZ, I., 1987. Fast
imaging of CSF flow-motion patterns using steady-state free precession (SSFP), Investigative Radiology, 22, 761-771. LE BIHAN, D., BRETON, E., AUBIN, M. L., LALLEMAND, D. &
VIGNAUD, J., 1987. Study of cerebrospinal fluid dynamics by MRI of the intravoxel incoherent motions (IVIM). Journal of Neuroradiology, 14, 388-395. MANSFIELD, P., 1977. Multi-planar image formation using NMR spin echoes. Journal of Physics C: Solid State Physics, 10, L55-L58. MANSFIELD, P., CHAPMAN, B., DOYLE, M., TURNER, R., WORTHINGTON, B . S., FlRTH, J. L., HAY, S. M . &
COUPLAND, R. E., 1986. Observation of CSF and ventricular motion in the brain by real-time echo-planar imaging. Proceedings of the 5th Annual Meeting of the Society of Magnetic Resonance in Medicine, Montreal, Vol. 3 (The Society of Magnetic Resonance in Medicine, Berkeley, California) pp. 699-670. MARK, A. S., FEINBERG, D. A. & BRANT-ZAWASSKI, M. N.,
1987. Changes in size and magnetic resonance signal intensity of the cerebral CSF spaces during the cardiac cycle, as studied by gated, high resolution MRI. Investigative Radiology, 22, 290-297. O'CONNELL, J. E. A., 1943. Vascular factors in intra-cranial pressure and maintenance of CSF circulation. Brain, 66, 204. ORDIDGE, R. J., COXON, R., HOWSEMAN, A. M., CHAPMAN, B., TURNER, R., STEHLING, M. K. & MANSFIELD, P., 1988.
Snapshot head imaging at 0.5 T using the echo planar technique. Magnetic Resonance in Medicine, 8, 110-115. ORDIDGE, R. J., GUILFOYLE, D. N., GIBBS, P. & MANSFIELD, P.,
1989. Real-time flow measurements using echo-planar imaging. Proceedings of the 8th Annual Meeting of the Society of Magnetic Resonance in Medicine, Amsterdam, Vol. 2 (SMRM), p. 889. SINGER, J. R., 1978. NMR diffusion and flow measurements and an introduction to spin phase graphing. Journal of Physics E: Scientific Instrumentation, 11, 281-291. STEHLING, M. K., COXON, R., ORDIDGE, R. J., HOWSEMAN, A. M., CHAPMAN, B., TURNER, R., FIRTH, J. L. &
MANSFIELD, P., 1988. Ultrafast dynamic headscanning with EPI: selected clinical cases. Proceedings of the 2nd European Congress of NMR in Medicine and Biology, Berlin (European Society of Magnetic Resonance in Medicine and Biology, Berlin).
VERITY, P., 1972. Further investigations on pulsatile movements in the cerebrospinal fluid pathways. Ada Radiologica Diagnosis, 13, 496-521. FEINBERG, D. A. & MARK, A. S., 1987. Human brain motion and cerebrospinal fluid circulation demonstrated with MR velocity imaging. Radiology, 163, 793-799.
STEHLING, M. K., HOWSEMAN, A. M., ORDIDGE, R. J., CHAPMAN, B., TURNER, R., COXON, R., GLOVER, P.,
HOWSEMAN, A. M., CHAPMAN, B. & MANSFIELD, P., 1987. Slow
MANSFIELD, P. & COUPLAND, R. E., 1989. Whole-body echo-
motion and flow by echo-planar imaging. Proceedings of the 6th Annual Meeting of the Society of Magnetic Resonance in Medicine, New York, Vol. 2 (The Society of Magnetic Resonance in Medicine, Berkeley, California) p. 861.
STEHLING, M. K., FIRTH, J. L., WORTHINGTON, B. S., COXON, R., ORDIDGE, R. J., BLAMIRE, A. M., GIBBS, P. &
planar MR imaging at 0.5 T. Radiology, 170, 257-263. MANSFIELD, P., Echo-planar imaging the CNS. Part I: technique and procedure (in press).
HOWSEMANN, A. M., STEHLING, M. K., CHAPMAN, B., COXON, R., TURNER, R., ORDIDGE, R. J., CAWLEY, M. G., GLOVER, P., MANSFIELD, P. & COUPLAND, R. E., 1988. Improvements
WEHRLI, F. W., MACFALL, J. R., AXEL, L., SHUTTS, D., GLOVER, G. H. & HERFKENS, R. J., 1984. Approaches to in-
in snap-shot nuclear magnetic resonance imaging. British Journal of Radiology, 61, 822-828.
plane and out-of-plane flow imaging. Non-invasive Medical Imaging, 1, 127-136.
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VOLUME 64 NUMBER 758
FEBRUARY 1991
The British Journal of Radiology Observation of cerebrospinal fluid flow with echo-planar magnetic resonance imaging By M. K. Stehling, MD, PhD, *J. L Firth, FRCS, tB. S. Worthington, BSc, D. N. Guilfoyle, PhD, R. J. Ordidge, PhD, R. Coxon, PhD, A. M. Blamire, BSc, P. Gibbs, BSc, *P. Bullock, FRCS and P. Mansfield, PhD, FRS Department of Physics, University of Nottingham and Departments of 'Neurosurgery and tAcademic Radiology, Queen's Medical Centre, Nottingham NG7 2RD, UK (Received April 1990 and in revised form August 1990) Keywords: Echo-planar magnetic resonance imaging, Cerebrospinal fluid
Abstract. Using echo-planar (EP) magnetic resonance imaging (MRI), cerebrospinal fluid (CSF) flow patterns have been demonstrated in the normal subject and patients with pathological conditions including communicating hydrocephalus, aqueduct stenosis and syringohydromyelia. Snap-shot imaging times of 128 ms allow detailed demonstration of transient intraventricular CSF flow patterns, which is not possible with conventional MRI. The potential of EPI as a method for qualitative and quantitative assessment of CSF dynamics is illustrated.
A number of different approaches have been made using conventional two-dimensional Fourier transform magnetic resonance imaging (2D-FT MRI) techniques to image cerebrospinal fluid flow within the ventricular system and basal cisterns (Bergstrand et al, 1985; Bradley et al, 1986; Jolesz et al, 1987). Superimposed on the slow overall circulation of cerebrospinal fluid (CSF) are respiratory and cardiac dependent pulsatile flow which can be identified on MR imaging by "time of flight" effects (Singer, 1978) as well as reversible and irreversible phase changes (Wehrli et al, 1984). Conventional MRI techniques, however, employ repetitive data acquisition over an extended period of time so that flow patterns can only be depicted as a weighted average over time. Even when time-resolved flow information has been obtained by means of cardiac gating, only regular and repetitive features of flow are captured and information about transient flow patterns is lost. The requirements for an ideal method of studying CSF flow in vivo would include the following: first, it should be non-invasive; secondly have no planar restrictions; thirdly be capable of gathering data very rapidly; and finally provide directional information and quantification of flow over the full range of values found in normal subjects and pathological conditions. Echo-planar imaging (EPI) is an ultrafast nuclear magnetic resonance technique able to produce snap-shot images in typically 30-100 ms (Mansfield, 1977). We have applied EPI operating in a real-time mode to Please address reprint requests to Professor P. Mansfield. Vol. 64, No. 758
observe CSF dynamics in the normal subject and several patients with pathological conditions including hydrocephalus and syringohydromyelia. The first observations of CSFflowby EPI and attempts to quantify slow flow have been reported previously (Mansfield et al, 1986; Howseman et al, 1987). The ability to depict CSF signal intensity changes with EPI allows demonstration of CSF flow phenomena with high spatial and temporal resolution. This allows a detailed description of individual flow patterns and their evolution in time. The simulation of flow phenomena in phantoms provides a basis for qualitative interpretation of the CSF flow patterns which are observed in vivo. Technique
Imaging was carried out on our home-built 0.52 Tesla EPI scanner. An actively shielded whole-body gradient coil system was used in conjunction with a purpose-built head-size birdcage RF coil. The pulse sequence and A>space diagrams in Fig. 1 show how an EP image is acquired. The rapidly switched frequency encoding j-gradient creates 128 gradient echoes in 128 ms. Each gradient echo corresponds to one of the 128 lines in A>space. Phase encoding is obtained through ^-gradient bursts (blips) at the ^-gradient zero-crossings. Full details of the modulus blipped echo-planar single shot technique (MBEST) as used for transaxial scanning is given elsewhere (Howseman et al, 1988; Ordidge et al, 1988; Stehling et al, 1989). For imaging in the coronal and sagittal planes, the 89
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Figure 1. MBEST and EPI (dashed) pulse sequence diagram (A) and fc-space trajectories (B). For coronal plane EPI, the rapidly switched frequency encoding gradient is along the >>-axis, while for sagittal EPI it is along the x-axis. The chemically selective phase (shaded) provides lipid/water proton signal suppression when required.
Figure 2. Six consecutive 64 ms MBEST snap-shots of circular flow in a 20 cm diameter water phantom. Dark areas indicate partially saturated spins (TR « 620 ms), moving within the image plane. In the first image of the sequence (TR = oo) flow, although present, is not detected. Bright areas are caused by flow components perpendicular to the image plane, resulting in flow related enhancement.
90
slice selective gradient is applied along the jc-axis and the j-axis respectively. The extent of the imaging plane along the z-axis is defined by the sensitive volume of the RF coil. This provides a reasonably sharp cut-off which avoids aliasing in the z-direction. Slice selection is followed by a standard EPI pulse sequence (Mansfield, 1977). This employs a non-blipped phase encoding gradient and creates the zig-zag fc-space trajectory shown dashed in Fig. IB. The constant low level phase encoding gradient was necessary in this case because the high inductance of the z-gradient coil prevented application of the z-gradient blips. All images are based on 128x128 pixel arrays with approximately 1.7 mm inplane resolution and a slice thickness of 10mm. Acquisition of a complete two-dimensional EP image takes 128 ms. For the creation of movie loops, triggered image acquisition was employed with 16 progessively delayed steps through the cardiac cycle triggered from a peripheral pulse monitor. The repetition time (TR) delay between consecutive frames was of the order of 2 s which allowed almost complete T, relaxation of brain tissue between shots. CSF proton spins were partially saturated and thus sensitized to flow through the imaging plane. Grey-white matter contrast in MBEST and EP images is based on the intrinsic T^-weighting of these techniques, caused by the delayed signal maximum of the echo-train (for full explanation see the following: Howseman et al, 1988; Ordidge et al, 1988; Stehling et al, 1989). To a first approximation the contrast in the MBEST images shown here is equivalent to that provided by a 3000/63 spin echo sequence. Results Flow phantoms
To verify the theoretical flow dependency of EPI two different phantoms were used to demonstrate the effects of bulk flow in EPI images. The British Journal of Radiology, February 1991
CSFflow shown by echo-planar MRI
Figure 3. Six 64 ms MBEST images demonstrating signal dephasing caused by turbulent in-plane flow. The flow patterns were induced by squirting 1 ml of water through a narrow nozzle into 150 ml of stagnant water.
Flow into the imaging plane was produced with the "swirling water" phantom. A simple cylindrical 20 cm diameter plastic bottle filled with tap water was spun about its longitudinal axis to establish circular flow and the contents of the bottle were then imaged. The eight 64 ms MBEST images shown in Fig. 2 were acquired with a TR of 620 ms between consecutive images. The maximum linear flow velocity at the perimeter of the bottle was approximately 30 cm/s. The high signal intensity spiral patterns in images 2-8 are caused by the introduction of fresh spins into the imaging plane by the component of flow perpendicular to it. These newly added spins provide an indication of the in-plane component of the flow. The absence of flow patterns in the first image, with flow already established but no preceding excitation, clearly indicates the Tx relaxation based nature of this phenomenon. Rapid in-plane flow was demonstrated with a phantom composed of two 150 ml plastic bottles connected by a 2 mm bore plastic tube. Approximately 1 ml of water was gently squeezed through the plastic tube from one bottle into the stagnant water of the bottle depicted in the images in Fig. 3. Images were obtained with incremental time delays after squeezing and show the development of a jet originating from the small nozzle at the end of the connecting tube. Turbulent flow within the jet causes spin dephasing and results in a signal void. Note the detailed patterns of turbulent flow in the upper part of the phantom. Vol. 64, No. 758
CSF flow A representative series of coronal images from a normal volunteer is shown in Fig. 4. These were taken through a single plane intersecting the cerebral hemispheres, brainstem and upper cervical cord. The CSF within the ventricular system, basal cisterns and subarachnoid pool around the cord appears bright. Sequential images triggered to the cardiac cycle show that in systole the signal form from the CSF at the foramen magnum disappears, indicating rapid CSF flow between the intracranial and intraspinal compartments. Pulsation of CSF within the cervical theca and basal cisterns is a phenomenon which was well known to neuroradiologists when carrying out Myodil myelography and cisternography (Du Boulay, 1966). This is strikingly displayed on the movie loop and with improvements in spatial resolution pulsatile movement of the brain parenchyma should be detectable. Evidence for vascular pulsation based brain motion has recently been demonstrated by MR velocity imaging (Feinberg & Mark, 1987). Complex flow patterns within the ventricles have been demonstrated in a patient with aqueduct stenosis. Figure 5 shows a movie loop of 16 coronal 128 ms acquisition time EP images 2 cm posterior to the foramina of Monro. Areas of high signal intensity are seen within the lateral ventricles which wax and wane. Peripheral to these are irregular bands of low signal intensity. The former represent flow perpendicular to the imaging 91
M. K. Stehling et al
Figure 4. Four snapshots from a 16 frame coronal EPI movie loop through the cerebrum and brainstem is shown. Signal void in the subarachnoid spaces at the foramen magnum is caused by rapid CSF flow. Vascular pulsation related brain movement is more obvious when the sequence is displayed as a movie loop. (Ref. 04503.)
plane, that is along the bodies of the ventricles, whereas the latter represent in-plane rapid flow, which is assumed to be secondary to the jet of CSF ejected through the foramina of Monro in systole. Eight frames from a transaxial 16 frame MBEST movie loop of the same patient are shown in Fig. 6 and again an area of signal attenuation is seen at the foramina of Monro during systole. As in the coronal movie loop, the flow pattern is more pronounced on the right side. These findings have been confirmed by preceding the MBEST sequence with a flow sensitizing sequence 92
(Ordidge et al, 1989) in order to obtain quantifiable flow information. The flow sensitizing gradient was applied in the z-direction, i.e. along the patient axis. The z-component of CSF flow is mapped in Fig. 7 for three different phases of the cardiac cycle. Figures 7A, 7B and 7C correspond approximately to Figs 6C, 6G and 6H respectively. For uniform flow velocity v within a pixel, the image signal intensity, /, is given by / oc sinfcv where k is a constant determined by the flow encoding sequence parameters. The flow map demonstrates general low level flow throughout the ventricles (blue), The British Journal of Radiology, February 1991
CSF flow shown by echo-planar MRI
Figure 5. Sixteen frame coronal EPI movie loop through the lateral and third ventricle, posterior to the foramen of Monro. The clock indicates the phase of the cardiac cycle with respect to the R wave, frame A. Flow along the body of the ventricles appears bright owing to flow related enhancement. Dark areas reflect rapid flow, originating at the foramen of Monro. (Ref. 04004.) and confirms the more rapid flow through the right foramen in systole (yellow and red). Note that the flow maximum is seen within the lateral ventricles. At the foramina, little signal is depicted, which may reflect turbulence resulting in loss of phase information. Figure 8 shows six coronal 128 ms acquisition time EP images in a patient with communicating hydrocephalus. The imaging plane intersects the lateral ventricles, aqueduct and fourth ventricle. During systole (frames A-C), a flame shaped area of signal void due to flow can be seen to originate from the aqueduct and extend into the upper part of the fourth ventricle. This confirms that the aqueduct is patent. The flow plume decays away in frames D - F during diastole. Figure 9 shows all 16 frames of a sagittal EPI movie loop in a patient with syringohydromyelia. Multiple areas of signal attenuation are seen in the fluid Vol. 64, No. 758
contained within the thin walls of the syrinx. These areas of signal loss indicate complex flow patterns within the fluid contained in the central cavity. Complex flow of CSF within syrinx cavities in five patients was also found by Le Bihan et al (1987), using the technique of mapping intravoxel incoherent motion.
Discussion Approximately 500 ml of CSF are secreted each day, largely by the choroid plexus within each lateral ventricle, and this circulates through the ventricular system and the cerebral and spinal subarachnoid systems before being absorbed by the arachnoid villi which are associated with the major dural venous sinuses. Superimposed on the slow background of circulation of CSF are respiratory and cardiac depen93
M. K. Stehling et al
Figure 6. Eight transaxial MBEST images at the foramina of Monro of the same case as in Fig. 5. Signal enhancement due to flow is demonstrated at the foramina in systole (frames G and H). (Ref. 04005.)
dent pulsatileflows.The mechanisms of CSF propulsion along these pathways are still incompletely understood. Cardiac dependent CSF motion occurs secondarily to cerebral perfusion. The existence of a third ventricular pump has been postulated (O'Connell, 1943) and much support for this hypothesis has been provided through observations made during pneumoencephalography (Du Boulay et al, 1972). In a recent study in normal individuals using gated high resolution MRI (Mark et al, 1987), the flow results were best explained by postulating a synchronous pulsatile flow of CSF at the foramen
of Monro and the aqueduct with an antegrade flow during systole and a retrograde but smaller flow during diastole, giving a net antegrade flow of CSF which enters the basal cisterns. The observation of pulsatile flow at the foramen of Monro suggests that the lateral ventricles do play a part in generating CSF flow, perhaps via expansion of the choroid plexus. Certainly considerable motion of CSF occurs within the lateral ventricles in pathological conditions, as we have observed in several cases in addition to the patient with aqueduct stenosis reported above.
Figure 7. Flow maps obtained at different phases of the cardiac cycle in the same patient as Figs 5 and 6: (A) diastole; (B) early systole; (C) mid-systole. Flow sensitization is along the z-axis or patients axis, i.e. in a direction perpendicular to the plane of the flow maps. Theflowvelocity is proportional to arcsin(T), where / is the signal intensity in the map (blue, low intensity; white, high intensity). Flow is more pronounced in the right foramina of Monro, in accordance with theflowpatterns in the standard MBEST images of Figs 5 and 6. (Ref. 04005.) 94
The British Journal of Radiology, February 1991
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Figure 9. Sixteen frames of a sagittal EPI movie loop, showing intracavitary fluid flow in a syringohydromyelia. Areas of signal void indicate turbulent flow in eddies, which travel caudally during systole. Note the development of a jet in systole at the narrowed part of the spinal canal (arrow). (Ref. 21301.)
CSF flow shown by echo-planar MRI Conclusion
We have shown that EPI can be used to study flow patterns in the CSF pathways with high spatial and temporal resolution. In the MBEST technique, both real and imaginary components of the NMR signal are collected, from which magnitude and phase information can be derived and this can be used to study transient, complex CSFflowpatterns in real time. Using aflowencoding sequence (Ordidge et al, 1989), we have produced coronal maps indicating CSFflowin the lateral ventricles of a patient with aqueduct stenosis. In these results localized flow is a direct and quantifiable function of localized signal intensity. Our results indicate that EPI is able to provide both qualitative and quantitative information in real-time. This could be of value for studying CSF flow dynamics in both normal and abnormal situations. Acknowledgments We thank the Medical Research Council, the Department of Health and the British Heart Foundation for their support of the echo-planar imaging programme. M.St. thanks the Deutsche Forschungsgemeinschaft for a stipend. We are grateful to Mark Symms for help with data processing and photography. References BERGSTRAND, G., BERGSTROM, M., NORDELL, B., STRAHLBERG, F., ERICSSON, A., HEMMINGSON, A., SOERKER, G., THUOMAS,
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JOLESZ, F. A., PARZ, S., HAWKES, R. C. & LOPEZ, I., 1987. Fast
imaging of CSF flow-motion patterns using steady-state free precession (SSFP), Investigative Radiology, 22, 761-771. LE BIHAN, D., BRETON, E., AUBIN, M. L., LALLEMAND, D. &
VIGNAUD, J., 1987. Study of cerebrospinal fluid dynamics by MRI of the intravoxel incoherent motions (IVIM). Journal of Neuroradiology, 14, 388-395. MANSFIELD, P., 1977. Multi-planar image formation using NMR spin echoes. Journal of Physics C: Solid State Physics, 10, L55-L58. MANSFIELD, P., CHAPMAN, B., DOYLE, M., TURNER, R., WORTHINGTON, B . S., FlRTH, J. L., HAY, S. M . &
COUPLAND, R. E., 1986. Observation of CSF and ventricular motion in the brain by real-time echo-planar imaging. Proceedings of the 5th Annual Meeting of the Society of Magnetic Resonance in Medicine, Montreal, Vol. 3 (The Society of Magnetic Resonance in Medicine, Berkeley, California) pp. 699-670. MARK, A. S., FEINBERG, D. A. & BRANT-ZAWASSKI, M. N.,
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