- Email: [email protected]
Shunt surgery effects on cerebrospinal fluid flow across the aqueduct of Sylvius in patients with communicating hydrocephalus
Journal of Clinical Neuroscience 16 (2009) 514–518
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Shunt surgery effects on cerebrospinal fluid flow across the aqueduct of Sylvius in patients with communicating hydrocephalus Pooja Abbey a,*, Paramjit Singh b, N. Khandelwal b, K.K. Mukherjee c a
Radiology, All India Institute of Medical Sciences, New Delhi, India Department of RadioDiagnosis and Imaging, Post Graduate Institute of Medical Education and Research, Chandigarh, India c Department of Neurosurgery, Post Graduate Institute of Medical Education and Research, Chandigarh, India b
a r t i c l e
i n f o
Article history: Received 4 April 2008 Accepted 18 May 2008
Keywords: Cerebrospinal fluid flow Aqueduct of Sylvius Cine cardiac-gated phase contrast MRI Shunt effect on CSF flow
a b s t r a c t We aimed to visualize and quantify the flow of cerebrospinal fluid (CSF) across the aqueduct of Sylvius in patients with communicating hydrocephalus using phase contrast MRI, and to evaluate the effect of ventriculoperitoneal (VP) shunt surgery on flow. We investigated aqueductal CSF flow using cine cardiacgated phase contrast MRI in 10 normal volunteers and 10 patients with communicating hydrocephalus (who underwent VP shunt surgery). For qualitative evaluation, we used an in-plane phase contrast sequence in the midsagittal plane. Quantitative through-plane measurements were performed in the axial plane perpendicular to the aqueduct. The aqueduct area ranged from 0.02 cm2 to 0.27 cm2 in the shunt group; and from 0.01 cm2 to 0.04 cm2 in the control group (p < 0.05). Aqueductal stroke volume (mean, standard deviation SD) ranged from 1.9 lL to 33.17 lL (17.41 lL, 10.1132) in the control group; and from 5.63 lL to 256 lL (87.20 lL, 79.0383) in the study group. Post-operatively the aqueductal stroke volume reduced significantly, ranging from 0.60 lL to 48.77 lL (13.19 lL, 18.08) (p < 0.05). Peak systolic velocity (PSV) values in the patients before shunt surgery ranged from 1.05 cm/s to 8.10 cm/s ( 4.39cm/s, 2.7619) and peak diastolic velocities (PDV) ranged from 0.62 cm/s to 5.16 cm/s (3.33 cm/ s, 1.4451). Post- shunt; PSV values ranged from 0.37 cm/s to 3.90 cm/s (1.78 cm/s, 1.5143) and PDV range was 0.32 cm/s to 4.43 cm/s (1.78 cm/s, 1.6782). The post-operative reduction in velocity was significant (p < 0.05). Thus, the aqueductal CSF flow after VP shunt was similar to flow in healthy volunteers. Ó 2008 Elsevier Ltd. All rights reserved.
1. Introduction Hydrocephalus is one of the most common disorders treated by neurosurgeons because it is a manifestation or sequela of many neurological diseases. Communicating hydrocephalus results from an obstruction distal to the outlet foramina of the fourth ventricle. Communicating hydrocephalus may result from several aetiologies (including meningeal infection, subarachnoid hemorrhage, trauma, carcinomatous meningitis and after intracranial surgery). MRI has revolutionised the non-invasive evaluation of cerebrospinal fluid (CSF) flow. Techniques that use cardiac-gating are more sensitive than routine MRI to evaluate CSF flow.1 Flow velocity can be estimated by the degree of signal loss in the flow void seen on routine gradient echo images. Cine phase-contrast MRI has been used increasingly since the late 1990s for evaluating cranial and spinal CSF flow.2 This technique is extremely sensitive, even to slow flow; and provides the potential to quantify flow non-
* Corresponding author. Present address: C/O Dr D. M. Abbey, S-11 Panchshila Park, New Delhi 110017, India. Tel.: +91 98 1097 6589/+91 98 6897 2835. E-mail address: [email protected] (P. Abbey). 0967-5868/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2008.05.009
invasively. Cardiac cycle-related variations in the cerebral blood volume produce bidirectional oscillatory movement of CSF within the craniospinal axis.1–6 During systole, the net inflow of blood increases the intracranial volume and produces craniocaudal (systolic) CSF flow. During diastole, the net outflow of blood decreases the intracranial volume and promotes caudocranial (diastolic) flow. Phase-contrast MRI can display this pulsatory CSF motion and allows measurement of its amplitude.1–6 We aimed to evaluate and compare the various parameters of CSF flow across the aqueduct of Sylvius in normal volunteers and in patients with communicating hydrocephalus, before and after ventriculoperitoneal (VP) shunt surgery; and to correlate changes in flow dynamics with post-surgical clinical improvement in these patients. 2. Materials and methods CSF flow parameters were evaluated in 2 groups of individuals. The controls (group 1) comprised 10 individuals who were normotensive and had no clinical or radiological signs of abnormalities in CSF circulation. All these individuals had a normal
P. Abbey et al. / Journal of Clinical Neuroscience 16 (2009) 514–518
MRI of the brain. Controls were age and sex matched with the patients in the study group. The study group (group 2) comprised 10 patients who presented with symptoms and radiological findings of communicating hydrocephalus of various etiologies (6 postmeningitic, 1 post-traumatic, 1 post-operative for internal carotid artery (ICA) aneurysm and 2 idiopathic). All 10 patients were subjected to CSF flow diversion in the form of a VP shunt. All patients in the study group underwent MRI scans before and after shunt surgery. Post-operative MRI was performed between 2 days and 20 days after surgery. Symptoms and signs were assessed pre-operatively and post-operatively. MRI studies were done on a 1.5 T MR unit (Magnetom Vision, Siemens, Erlangen, Germany). In all cases, axial proton density (PD) and T2-weighted turbo spin echo (SE) images (TR/TE 3000/102 ms; 2 excitations) were obtained (5 mm slice thickness with 20% interslice gap) to evaluate the ventricular system. We then performed cine phase-contrast MRI using prospective cardiac gating to evaluate CSF flow. For a qualitative assessment of CSF flow, phase contrast MR images were acquired in the midsagittal plane using a flash two-dimensional (2D) gradient echo sequence (TR 70 ms, TE 15.5, flip angle 10°, pixel size 1.3 mm 0.98 mm, matrix 144 256). The screening time varied between 3.5 min and 6.0 min depending upon the heart rate. As a convention, on midsagittal MRI, cranial flow was seen as a bright signal and caudal flow as a dark signal. The quantitative flow parameters were acquired in an axial plane perpendicular to the long axis of the aqueduct, passing through its mid portion (parameters: TR 100 ms, TE 12 ms, flip angle 0°, FOV 220, pixel size 0.86 mm 0.43 mm, matrix 224 512). The scanning time varied from 7 min to 12 min. On axial MRI, the cranial flow was seen as a dark signal and the caudal flow as a bright signal. The flow velocity sensitivity (velocity encoding) was set at 20 cm/s. An annular region of interest (ROI) was placed upon the aqueduct, encircling its entire area, with the aid of a mouse driven cursor. Using a flow quantification package (Siemens Magnetom Vision, Numaris VB31B software, Siemens, Medical Solutions, Erlangen, Germany), the following six CSF flow parameters were assessed: (i) area of the aqueduct (cm2); (ii) aqueductal stroke volume (mm3/lL); (iii) peak systolic volume (PSV) (cm/s) (negative values due to flow in craniocaudal direction, by convention); (iv) peak diastolic velocity (PDV) (cm/s) (positive values due to caudocranial flow); (v) mean velocity (MV) (cm/s); and (vi) mean flow (MF) (cm3/s). These quantitative CSF flow parameters were compared between the control group and the patients in the study group, before and after shunt surgery. 3. Results There were seven males and three females in each group, and their ages ranged from 17 to 50 years (50% between 21 years and
515
30 years). The various etiologies of communicating hydrocephalus in the 10 patients were: sequelae of meningitis (6), post-traumatic (1), post-operative (1) and idiopathic (2). The members of the control group did not have any clinical or radiological evidence of abnormalities in the ventricular system or CSF circulation. The CSF flow pattern was similar in all patients and controls. CSF systole (motion in craniocaudal direction) was observed to start in the upper cervical subarachnoid space and then in the basal cisterns. Systolic flow within the ventricles and the aqueduct was slightly delayed compared to that of the cisterns. CSF diastole occurred first in the upper cervical subarachnoid space followed by flow reversal in the prepontine cistern, aqueduct and ventricles. In 6 out of 10 patients with communicating hydrocephalus, more turbulent flow was observed in the fourth ventricle in the form of areas of signal dropout and aliasing. These patients, on quantitative evaluation, had hyperdynamic flow in the form of high CSF aqueductal stroke volumes. In these patients, post VP shunt, turbulence was reduced in the fourth ventricle (Fig. 1). The area of the aqueduct (mean, standard deviation [SD]) ranged from 0.01 cm2 to 0.04 cm2 (0.02 cm2, 0.0097) in the control group, and 0.02 cm2 to 0.27 cm2 (0.10 cm2, 0.894) in the study (hydrocephalus) group (Table 1). In 8/10 patients with hydrocephalus; the area was more than 0.04 cm2 (i.e. greater than the maximum in the control group). The difference in area between the patient and control group was statistically significant (p < 0.05). The area of the aqueduct decreased post-shunt in 9/10 patients. In one patient, the post-shunt area was higher than the pre-operative value (0.04 cm2 vs. 0.02 cm2). In control patients, the aqueductal stroke volume (mean, SD) ranged from 1.9 lL to 33.17 lL (17.41, 10.1132), and in the study group, 5.63 lL to 256.36 lL (87.20, 79.0383) (Table 2). Post-operatively, aqueductal stroke volume was reduced significantly in all 10 patients (p < 0.05) (range 0.60–48.77 lL) (13.91, 18.08) (Fig. 2). The post-shunt values were not statistically different from the stroke volumes observed in the controls. Among the patients with communicating hydrocephalus, two categories were observed: 6 out of 10 had high pre-shunt values of aqueductal CSF stroke volume; while the remaining 4 had values that were within the ‘‘normal” range. In all 6 patients with high aqueductal CSF stroke volumes, there was post-surgical improvement; of the 4 patients with values in the normal range, only 1 showed improvement. However, this difference was not statistically significant (p = 0.066). Prominent CSF flow voids were seen in 5/10 patients and all of them had high values of aqueductal stroke volume. One patient, despite having a high CSF stroke volume on quantitative evaluation, did not show prominence of flow void on PD/T2-weighted MRI.
Fig. 1. Axial proton density MRI of patient 1 showing (arrows) prominent flow void through (A) the aqueduct pre-shunt, (B) the fourth ventricle pre-shunt and (C) a reduction in flow void post-shunt.
516
P. Abbey et al. / Journal of Clinical Neuroscience 16 (2009) 514–518
Table 1 Area of the aqueduct (cm2) in patients with hydrocephalus and healthy individuals Patients No. 1 2 3 4 5 6 7 8 9 10
Controls Age (y)/ gender
Area pre-shunt
Area post-shunt
No.
26/M 23/M 45/M 21/F 26 /M 40/F 23/F 17/M 40/M 50/M
0.12 0.27 0.05 0.08 0.05 0.08 0.05 0.02 0.02 0.06
0.07 0.05 0.02 0.05 0.02 0.01 0.03 0.04 0.01 0.04
1 2 3 4 5 6 7 8 9 10
Age (y)/ gender
Area
26/M 23/M 45/M 21/F 26/M 40/F 23/F 17/M 40/M 50/M
0.01 0.03 0.03 0.02 0.01 0.03 0.02 0.03 0.04 0.02
Peak CSF velocities, both systolic (PSV) and diastolic (PDV), showed a wide range in both groups (Table 3). In the control group, PSVs ranged (mean, SD) from 1.23 cm/s to 4.87 cm/s (3.24 cm/s, 1.0795) and diastolic velocities ranged from 1.23 cm/s to 3.38 cm/s (2.48 cm/s, 0.6012). The peak pre-shunt velocities in the patients with hydrocephalus were not significantly different from values observed in the controls (Table 4). The PSV range (mean, SD) was from 1.05
Table 2 Aqueductal stroke volume (mm3 or lL) in patients with hydrocephalus and healthy individuals Patients
Controls
No.
Age (y)/gender
Volume pre-shunt
Volume post-shunt
No.
Age (y)/ gender
Volume
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26 /M 40/F 23/F 17/M 40/M 50/M
256.36 139.04 59.12 114.4 94.66 142.66 24.85 5.63 13.3 21.94
48.77 36.56 2.67 31.43 0.98 0.66 2.71 2.4 0.6 12.29
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26/M 40/F 23/F 17/M 40/M 50/M
7.24 26.14 28.88 1.9 8.67 21.60 12.61 18.17 33.17 15.74
cm/s to 8.10 cm/s ( 4.39 cm/s, 2.7619) and values of PDV ranged from 0.62 cm/s to 5.16 cm/s (3.33 cm/s, 1.4451). The PSV values post-shunt ranged from 0.37 cm/s to 3.90 cm/s ( 1.78 cm/s, 1.5143) and PDV ranged from 0.32 cm/s to 4.43 cm/s (1.78 cm/s, 1.6782). Peak systolic and diastolic velocities decreased post-operatively in 9 out of 10 patients, which was statistically significant
Fig. 2. Cine phase-contrast MRI of patient 2 showing (A) the placement of region of interest (ROI) on an axial section (arrow) and (C) the cerebrospinal fluid (CSF) flow through the aqueduct post-shunt (arrow) on a sagittal section. (B) Pre-shunt CSF flow wave forms (stroke volume 59.12 lL) and (D) post-shunt measurements (stroke volume 2.67 lL).
517
P. Abbey et al. / Journal of Clinical Neuroscience 16 (2009) 514–518 Table 3 Peak systolic and diastolic velocities (cm/s) in patients and controls Patients
Controls
No.
Age (y)/ gender
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26 /M 40/F 23/F 17/M 40/M 50/M
Pre-shunt
Post-shunt
PSV
PSV
8.10 1.05 7.17 6.58 2.56 7.83 2.66 1.43 2.33 4.22
PDV +5.16 +3.08 +2.95 +4.93 +0.62 +4.72 +2.35 +2.04 +4.21 +3.27
3.90 3.39 0.96 3.13 0.40 0.87 0.44 0.37 0.74 3.64
PDV
No.
Age (y)/ gender
+3.90 +4.43 +0.90 +2.98 +0.43 +0.32 +0.39 +0.52 +0.51 +3.37
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26/M 40/F 23/F 17/M 40/M 50/M
PSV
PDV
2.27 3.16 4.87 1.23 3.48 4.25 2.91 2.39 3.85 3.99
+2.07 +2.61 +3.09 +1.23 +2.44 +2.36 +2.75 +2.78 +3.38 +2.10
PDV = peak diastolic velocity, PSV = peak systolic velocity, ‘‘–” sign = craniocaudal flow, ‘‘+” sign = caudocranial flow.
(p < 0.05). Peak CSF velocities were <5 cm/s in all controls; but in 4 out of 10 patients with hydrocephalus, velocities were >6 cm/s, which suggested hyperdynamic flow through the aqueduct (Table 4). The pre-shunt study group demonstrated higher values of mean flow (range 0.00 cm3/s to 0.44 cm3/s) (Table 4). In 7/10 patients, the mean CSF flow was >0.02 cm3/s. In these 7 patients, the mean flow rate was reduced post-shunt, but the difference was not statistically significant. 4. Discussion The non-invasive evaluation of CSF flow using MRI has evolved from visual qualitative techniques to a quantitative technique using cine phase-contrast CSF velocity MR imaging. Many authors have evaluated CSF flow dynamics across the aqueduct of Sylvius in healthy individuals and in patients with known or suspected CSF circulation disorders.1,4,7–13 Based on the clinical significance of detected CSF abnormalities, various authors have predicted which patients with hydrocephalus are likely to improve following CSF diversion.8,10–14,16–18 In 1991 Bradley et al. reported a highly significant association between a prominent CSF flow void in the cerebral aqueduct and a favorable response to surgery (CSF diversion).14 Our experience was similar. However, in 1996, Bradley et al. found no statistically significant association between flow void and response to CSF diversion.17 The measurement of flow void is highly dependent on acquisition parameters as well as the technical characteristics of MRI systems (e.g. gradient strength). In addition; evaluation of
the flow void is subjective, possibly rendering it a less sensitive predictor. In our study, the PSVs and PDVs, mean velocity and aqueductal CSF stroke volume demonstrated marked variation between individuals in both the study and the control groups. There was no correlation with the age or sex of the individuals. These findings are consistent with previous reports.6,9,15,19 In the patients with hydrocephalus, the aqueduct area was significantly greater than in the controls, and post-shunt values were not significantly different from those of the control group. These results are similar to Henry-Feugeas et al.20 and Bradley et al.19 In two of our patients, the aqueduct completely collapsed postoperatively. This made placement of the ROI over the aqueduct difficult, and subsequent evaluation of the quantitative flow parameters became subject to error. The resistance to CSF flow through the aqueduct is inversely proportional to the fourth power of its radius; therefore, small changes in the size of the aqueduct cause large changes in CSF flow. The aqueductal CSF stroke volume is an average volume of CSF moving in a craniocaudal direction during systole and caudocranial direction during diastole. In 1996 Bradley et al. reported that patients with stroke volumes greater than 42 lL responded to shunting while 50% of the patients with stroke volume less than 42 lL did not respond.17 In our study group, 6 patients had high stroke volumes (>50 lL) and the other 4 had stroke volume values that fell in the ‘‘normal” range. After shunt surgery, the stroke volumes reduced significantly (0.6–48.77 lL), which indicated a functional VP shunt. The difference between stroke volumes in patients and controls was statistically significant, and so was the reduction in stroke volumes post CSF diversion. In our study, a cut-off value of P50 lL of the aqueductal CSF stroke volume defined hyperdynamicity of CSF flow, whereas values between 35 lL and 50 lL constituted the intermediate or the ‘‘grey” zone. Our observation of clinical improvement in 5 out of 6 patients with high stroke volumes corroborates with previous reports.21 However; in our study, the difference was not statistically significant (p = 0.066). Our observation of a wide range of peak CSF velocities through the aqueduct is in accordance with previous reports.6,9,11,15,19 Although peak velocity was not a very good parameter for differentiating patients with hydrocephalus from normal individuals, amplitudes greater than 6 cm/s suggested communicating hydrocephalus with hyperdynamic flow. After shunt surgery, peak velocity was reduced in 9 out of 10 patients. We observed greater CSF velocities in craniocaudal direction (in systole) than caudocranial direction (diastole) in both the study and control groups. In addition, the amplitudes of systolic velocity peaks were greater than amplitudes of diastolic velocity peaks in 9/ 10 controls and 7/10 cases of hydrocephalus. Similar observations have been reported previously.6,19
Table 4 Mean velocity (cm/s) and mean flow (cm3/s) of pre-shunt and post-shunt cerebrospinal fluid (Craniocaudal flow is negative by convention) Patient
Controls Pre-shunt
No.
Age (y)/gender
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26 /M 40/F 23/F 17/M 40/M 50/M
Mean velocity 0.89 0.72 0.88 0.63 0.28 0.67 0.03 0.03 0.01 0.15
Post-shunt Mean flow 0.11 0.20 0.05 0.05 0.07 0.05 0.00 0.00 0.44 0.01
Mean velocity 0.16 0.17 0.06 0.15 0.02 0.21 0.06 0.07 0.02 0.27
Mean flow 0.04 0.01 0.00 0.01 0.00 0.00 0.00 0.00 0.00 0.02
No.
Age (y)/gender
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26/M 40/F 23/F 17/M 40/M 50/M
Mean velocity 0.52 0.48 0.60 0.10 0.79 0.50 0.34 0.22 0.32 0.41
Mean flow 0.00 0.01 0.02 0.00 0.01 0.01 0.01 0.01 0.01 0.01
518
P. Abbey et al. / Journal of Clinical Neuroscience 16 (2009) 514–518
5. Conclusion In conclusion, the qualitative and quantitative assessment of CSF flow using phase-contrast MRI can provide information about various flow parameters in normal individuals and also demonstrate altered flow dynamics in patients with communicating hydrocephalus. Increased aqueductal CSF stroke volume in patients with hydrocephalus predicts the likelihood of clinical improvement post CSF diversion. Repeat evaluation after shunt surgery helps establish how well the shunt system is functioning. CSF flow parameters in patients with hydrocephalus post VP shunt are similar to those in healthy subjects.
References 1. Nitz WR, Bradley Jr WG, Watanabe AS, et al. Flow dynamics of cerebrospinal fluid: assessment with phase contrast velocity MR imaging performed with retrospective cardiac gating. Radiology 1992;183:395–405. 2. Levy LM, Di Chiro G. MR phase imaging and cerebrospinal fluid flow in the head and spine. Neuroradiology 1990;32:399–406. 3. Quencer RM, Post MJ, Hinks RS. Cine MR in the evaluation of normal and abnormal CSF flow: intracranial and intraspinal stiudies. Neuroradiology 1990;32:371–91. 4. Henry–Feugeas MC, Idy-Peretti I, Blanchet B, et al. Temporal and spatial assessment of normal cerebrospinal fluid dynamics with MR imaging. Magn Reson Imaging 1993;11:1107–18. 5. Bhadelia RA, Bogdan AR, Wolpaert SM. Analysis of cerebrospinal fluid flow wave forms with gated phase-contrast MR velocity measurements. Am J Neuroradiol 1995;16:389–400. 6. Bhadelia RA, Bogdan AR, Kaplan RF, et al. Cerebrospinal fluid pulsation amplitude and its quantitative relationship to cerebral blood flow pulsations: a phase-contrast MR flow imaging study. Neuroradiology 1997;39:258–64. 7. Parkkola RK, Komu MES, Aarimaa TM, et al. Cerebrospinal fluid in children with normal and dilated ventricles studied by MR imaging. Acta Radiol 2001;42:33–8.
8. Bradley Jr WG, Scalzo D, Queralt J, et al. Normal pressure hydrocephalus: evaluation with cerebrospinal fluid flow measurements at MR imaging. Radiology 1996;198:523–9. 9. Gideon P, Thomsen C, Stahlberg F, et al. Cerebrospinal fluid production and dynamics in normal aging: a MRI phasemapping study. Acta Neurol Scand 1994;89:362–6. 10. Jacobson EE, Fletcher DF, Morgan MK. Fluid dynamics of the cerebral aqueduct. Pediatr Neurosurg 1996;24:229–36. 11. Kim DS, Choi JU, Huh R, et al. Quantitative assessment of cerebrospinal fluid hydrodynamics using a phase-contrast cine MR image in hydrocephalus. Childs Nerv Syst 1999;15:461–7. 12. Schroeder HWS, Schweim C, Schweim KH, et al. Analysis of aqueductal cerebrospinal fluid flow after endoscopic aqueductoplasty by using cine phasecontrast magnetic resonance imaging. J Neurosurg 2000;93:237–44. 13. Parkkola RK, Komu MES, Kotilainen EM, et al. Cerebrospinal fluid flow in patients with dilated ventricles studied with MR imaging. Eur Radiol 2000;10:1442–6. 14. Bradley WG, Whitemore AR, Watanabe AS, et al. Association of deep white matter infarction with chronic communicating hydrocephalus: implications regarding the possible origin of normal pressure hydrocephalus. Am J Neuroradiol 1991;12:31–9. 15. Gideon P, Stahlberg F, Thomsen C, et al. Cerebrospinal fluid flow and production in patients with normal pressure hydrocephalus studied by MRI. Neuroradiology 1994;36:210–5. 16. Mascalchi M, Arnetoli G, Inzitari D, et al. Cine-MR imaging of aqueductal CSF flow in normal pressure hydrocephalus syndrome before and after CSF shunt. Acta Radiol 1993;34:586–92. 17. Bradley WG, Kortman KE, Burgoyne B. Flowing cerebrospinal fluid in normal and hydrocephalic states: appearance on MR images. Radiology 1996;159:611–6. 18. Barcena A, Mestre C, Canizal JM, et al. Idiopathic normal pressure hydrocephalus: analysis of factors related to cerebrospinal fluid dynamics determining functional prognosis. Acta Neurochir 1997;139: 933–41. 19. Bradley WG, Whitemore A, Jinkins JR, et al. Cerebrospinal fluid flow patterns in hydrocephalus: correlation of clinical and phantom studies using MR imaging. Radiology 1987;165:78–9. 20. Henry-Feugeas MC, Idy-Peretti I, Baledent O, et al. Cerebrospinal fluid flow waveforms: MR analysis in chronic adult hydrocephalus. Invest Radiology 2001;36:146–54. 21. Borgsen SE, Gjerris F, Sorensen SC. Cerebrospinal fluid conductance and compliance of the cranial spinal space in normal pressure hydrocephalus. Neurosurg 1979;51:521–5.
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Shunt surgery effects on cerebrospinal fluid flow across the aqueduct of Sylvius in patients with communicating hydrocephalus Pooja Abbey a,*, Paramjit Singh b, N. Khandelwal b, K.K. Mukherjee c a
Radiology, All India Institute of Medical Sciences, New Delhi, India Department of RadioDiagnosis and Imaging, Post Graduate Institute of Medical Education and Research, Chandigarh, India c Department of Neurosurgery, Post Graduate Institute of Medical Education and Research, Chandigarh, India b
a r t i c l e
i n f o
Article history: Received 4 April 2008 Accepted 18 May 2008
Keywords: Cerebrospinal fluid flow Aqueduct of Sylvius Cine cardiac-gated phase contrast MRI Shunt effect on CSF flow
a b s t r a c t We aimed to visualize and quantify the flow of cerebrospinal fluid (CSF) across the aqueduct of Sylvius in patients with communicating hydrocephalus using phase contrast MRI, and to evaluate the effect of ventriculoperitoneal (VP) shunt surgery on flow. We investigated aqueductal CSF flow using cine cardiacgated phase contrast MRI in 10 normal volunteers and 10 patients with communicating hydrocephalus (who underwent VP shunt surgery). For qualitative evaluation, we used an in-plane phase contrast sequence in the midsagittal plane. Quantitative through-plane measurements were performed in the axial plane perpendicular to the aqueduct. The aqueduct area ranged from 0.02 cm2 to 0.27 cm2 in the shunt group; and from 0.01 cm2 to 0.04 cm2 in the control group (p < 0.05). Aqueductal stroke volume (mean, standard deviation SD) ranged from 1.9 lL to 33.17 lL (17.41 lL, 10.1132) in the control group; and from 5.63 lL to 256 lL (87.20 lL, 79.0383) in the study group. Post-operatively the aqueductal stroke volume reduced significantly, ranging from 0.60 lL to 48.77 lL (13.19 lL, 18.08) (p < 0.05). Peak systolic velocity (PSV) values in the patients before shunt surgery ranged from 1.05 cm/s to 8.10 cm/s ( 4.39cm/s, 2.7619) and peak diastolic velocities (PDV) ranged from 0.62 cm/s to 5.16 cm/s (3.33 cm/ s, 1.4451). Post- shunt; PSV values ranged from 0.37 cm/s to 3.90 cm/s (1.78 cm/s, 1.5143) and PDV range was 0.32 cm/s to 4.43 cm/s (1.78 cm/s, 1.6782). The post-operative reduction in velocity was significant (p < 0.05). Thus, the aqueductal CSF flow after VP shunt was similar to flow in healthy volunteers. Ó 2008 Elsevier Ltd. All rights reserved.
1. Introduction Hydrocephalus is one of the most common disorders treated by neurosurgeons because it is a manifestation or sequela of many neurological diseases. Communicating hydrocephalus results from an obstruction distal to the outlet foramina of the fourth ventricle. Communicating hydrocephalus may result from several aetiologies (including meningeal infection, subarachnoid hemorrhage, trauma, carcinomatous meningitis and after intracranial surgery). MRI has revolutionised the non-invasive evaluation of cerebrospinal fluid (CSF) flow. Techniques that use cardiac-gating are more sensitive than routine MRI to evaluate CSF flow.1 Flow velocity can be estimated by the degree of signal loss in the flow void seen on routine gradient echo images. Cine phase-contrast MRI has been used increasingly since the late 1990s for evaluating cranial and spinal CSF flow.2 This technique is extremely sensitive, even to slow flow; and provides the potential to quantify flow non-
* Corresponding author. Present address: C/O Dr D. M. Abbey, S-11 Panchshila Park, New Delhi 110017, India. Tel.: +91 98 1097 6589/+91 98 6897 2835. E-mail address: [email protected] (P. Abbey). 0967-5868/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2008.05.009
invasively. Cardiac cycle-related variations in the cerebral blood volume produce bidirectional oscillatory movement of CSF within the craniospinal axis.1–6 During systole, the net inflow of blood increases the intracranial volume and produces craniocaudal (systolic) CSF flow. During diastole, the net outflow of blood decreases the intracranial volume and promotes caudocranial (diastolic) flow. Phase-contrast MRI can display this pulsatory CSF motion and allows measurement of its amplitude.1–6 We aimed to evaluate and compare the various parameters of CSF flow across the aqueduct of Sylvius in normal volunteers and in patients with communicating hydrocephalus, before and after ventriculoperitoneal (VP) shunt surgery; and to correlate changes in flow dynamics with post-surgical clinical improvement in these patients. 2. Materials and methods CSF flow parameters were evaluated in 2 groups of individuals. The controls (group 1) comprised 10 individuals who were normotensive and had no clinical or radiological signs of abnormalities in CSF circulation. All these individuals had a normal
P. Abbey et al. / Journal of Clinical Neuroscience 16 (2009) 514–518
MRI of the brain. Controls were age and sex matched with the patients in the study group. The study group (group 2) comprised 10 patients who presented with symptoms and radiological findings of communicating hydrocephalus of various etiologies (6 postmeningitic, 1 post-traumatic, 1 post-operative for internal carotid artery (ICA) aneurysm and 2 idiopathic). All 10 patients were subjected to CSF flow diversion in the form of a VP shunt. All patients in the study group underwent MRI scans before and after shunt surgery. Post-operative MRI was performed between 2 days and 20 days after surgery. Symptoms and signs were assessed pre-operatively and post-operatively. MRI studies were done on a 1.5 T MR unit (Magnetom Vision, Siemens, Erlangen, Germany). In all cases, axial proton density (PD) and T2-weighted turbo spin echo (SE) images (TR/TE 3000/102 ms; 2 excitations) were obtained (5 mm slice thickness with 20% interslice gap) to evaluate the ventricular system. We then performed cine phase-contrast MRI using prospective cardiac gating to evaluate CSF flow. For a qualitative assessment of CSF flow, phase contrast MR images were acquired in the midsagittal plane using a flash two-dimensional (2D) gradient echo sequence (TR 70 ms, TE 15.5, flip angle 10°, pixel size 1.3 mm 0.98 mm, matrix 144 256). The screening time varied between 3.5 min and 6.0 min depending upon the heart rate. As a convention, on midsagittal MRI, cranial flow was seen as a bright signal and caudal flow as a dark signal. The quantitative flow parameters were acquired in an axial plane perpendicular to the long axis of the aqueduct, passing through its mid portion (parameters: TR 100 ms, TE 12 ms, flip angle 0°, FOV 220, pixel size 0.86 mm 0.43 mm, matrix 224 512). The scanning time varied from 7 min to 12 min. On axial MRI, the cranial flow was seen as a dark signal and the caudal flow as a bright signal. The flow velocity sensitivity (velocity encoding) was set at 20 cm/s. An annular region of interest (ROI) was placed upon the aqueduct, encircling its entire area, with the aid of a mouse driven cursor. Using a flow quantification package (Siemens Magnetom Vision, Numaris VB31B software, Siemens, Medical Solutions, Erlangen, Germany), the following six CSF flow parameters were assessed: (i) area of the aqueduct (cm2); (ii) aqueductal stroke volume (mm3/lL); (iii) peak systolic volume (PSV) (cm/s) (negative values due to flow in craniocaudal direction, by convention); (iv) peak diastolic velocity (PDV) (cm/s) (positive values due to caudocranial flow); (v) mean velocity (MV) (cm/s); and (vi) mean flow (MF) (cm3/s). These quantitative CSF flow parameters were compared between the control group and the patients in the study group, before and after shunt surgery. 3. Results There were seven males and three females in each group, and their ages ranged from 17 to 50 years (50% between 21 years and
515
30 years). The various etiologies of communicating hydrocephalus in the 10 patients were: sequelae of meningitis (6), post-traumatic (1), post-operative (1) and idiopathic (2). The members of the control group did not have any clinical or radiological evidence of abnormalities in the ventricular system or CSF circulation. The CSF flow pattern was similar in all patients and controls. CSF systole (motion in craniocaudal direction) was observed to start in the upper cervical subarachnoid space and then in the basal cisterns. Systolic flow within the ventricles and the aqueduct was slightly delayed compared to that of the cisterns. CSF diastole occurred first in the upper cervical subarachnoid space followed by flow reversal in the prepontine cistern, aqueduct and ventricles. In 6 out of 10 patients with communicating hydrocephalus, more turbulent flow was observed in the fourth ventricle in the form of areas of signal dropout and aliasing. These patients, on quantitative evaluation, had hyperdynamic flow in the form of high CSF aqueductal stroke volumes. In these patients, post VP shunt, turbulence was reduced in the fourth ventricle (Fig. 1). The area of the aqueduct (mean, standard deviation [SD]) ranged from 0.01 cm2 to 0.04 cm2 (0.02 cm2, 0.0097) in the control group, and 0.02 cm2 to 0.27 cm2 (0.10 cm2, 0.894) in the study (hydrocephalus) group (Table 1). In 8/10 patients with hydrocephalus; the area was more than 0.04 cm2 (i.e. greater than the maximum in the control group). The difference in area between the patient and control group was statistically significant (p < 0.05). The area of the aqueduct decreased post-shunt in 9/10 patients. In one patient, the post-shunt area was higher than the pre-operative value (0.04 cm2 vs. 0.02 cm2). In control patients, the aqueductal stroke volume (mean, SD) ranged from 1.9 lL to 33.17 lL (17.41, 10.1132), and in the study group, 5.63 lL to 256.36 lL (87.20, 79.0383) (Table 2). Post-operatively, aqueductal stroke volume was reduced significantly in all 10 patients (p < 0.05) (range 0.60–48.77 lL) (13.91, 18.08) (Fig. 2). The post-shunt values were not statistically different from the stroke volumes observed in the controls. Among the patients with communicating hydrocephalus, two categories were observed: 6 out of 10 had high pre-shunt values of aqueductal CSF stroke volume; while the remaining 4 had values that were within the ‘‘normal” range. In all 6 patients with high aqueductal CSF stroke volumes, there was post-surgical improvement; of the 4 patients with values in the normal range, only 1 showed improvement. However, this difference was not statistically significant (p = 0.066). Prominent CSF flow voids were seen in 5/10 patients and all of them had high values of aqueductal stroke volume. One patient, despite having a high CSF stroke volume on quantitative evaluation, did not show prominence of flow void on PD/T2-weighted MRI.
Fig. 1. Axial proton density MRI of patient 1 showing (arrows) prominent flow void through (A) the aqueduct pre-shunt, (B) the fourth ventricle pre-shunt and (C) a reduction in flow void post-shunt.
516
P. Abbey et al. / Journal of Clinical Neuroscience 16 (2009) 514–518
Table 1 Area of the aqueduct (cm2) in patients with hydrocephalus and healthy individuals Patients No. 1 2 3 4 5 6 7 8 9 10
Controls Age (y)/ gender
Area pre-shunt
Area post-shunt
No.
26/M 23/M 45/M 21/F 26 /M 40/F 23/F 17/M 40/M 50/M
0.12 0.27 0.05 0.08 0.05 0.08 0.05 0.02 0.02 0.06
0.07 0.05 0.02 0.05 0.02 0.01 0.03 0.04 0.01 0.04
1 2 3 4 5 6 7 8 9 10
Age (y)/ gender
Area
26/M 23/M 45/M 21/F 26/M 40/F 23/F 17/M 40/M 50/M
0.01 0.03 0.03 0.02 0.01 0.03 0.02 0.03 0.04 0.02
Peak CSF velocities, both systolic (PSV) and diastolic (PDV), showed a wide range in both groups (Table 3). In the control group, PSVs ranged (mean, SD) from 1.23 cm/s to 4.87 cm/s (3.24 cm/s, 1.0795) and diastolic velocities ranged from 1.23 cm/s to 3.38 cm/s (2.48 cm/s, 0.6012). The peak pre-shunt velocities in the patients with hydrocephalus were not significantly different from values observed in the controls (Table 4). The PSV range (mean, SD) was from 1.05
Table 2 Aqueductal stroke volume (mm3 or lL) in patients with hydrocephalus and healthy individuals Patients
Controls
No.
Age (y)/gender
Volume pre-shunt
Volume post-shunt
No.
Age (y)/ gender
Volume
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26 /M 40/F 23/F 17/M 40/M 50/M
256.36 139.04 59.12 114.4 94.66 142.66 24.85 5.63 13.3 21.94
48.77 36.56 2.67 31.43 0.98 0.66 2.71 2.4 0.6 12.29
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26/M 40/F 23/F 17/M 40/M 50/M
7.24 26.14 28.88 1.9 8.67 21.60 12.61 18.17 33.17 15.74
cm/s to 8.10 cm/s ( 4.39 cm/s, 2.7619) and values of PDV ranged from 0.62 cm/s to 5.16 cm/s (3.33 cm/s, 1.4451). The PSV values post-shunt ranged from 0.37 cm/s to 3.90 cm/s ( 1.78 cm/s, 1.5143) and PDV ranged from 0.32 cm/s to 4.43 cm/s (1.78 cm/s, 1.6782). Peak systolic and diastolic velocities decreased post-operatively in 9 out of 10 patients, which was statistically significant
Fig. 2. Cine phase-contrast MRI of patient 2 showing (A) the placement of region of interest (ROI) on an axial section (arrow) and (C) the cerebrospinal fluid (CSF) flow through the aqueduct post-shunt (arrow) on a sagittal section. (B) Pre-shunt CSF flow wave forms (stroke volume 59.12 lL) and (D) post-shunt measurements (stroke volume 2.67 lL).
517
P. Abbey et al. / Journal of Clinical Neuroscience 16 (2009) 514–518 Table 3 Peak systolic and diastolic velocities (cm/s) in patients and controls Patients
Controls
No.
Age (y)/ gender
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26 /M 40/F 23/F 17/M 40/M 50/M
Pre-shunt
Post-shunt
PSV
PSV
8.10 1.05 7.17 6.58 2.56 7.83 2.66 1.43 2.33 4.22
PDV +5.16 +3.08 +2.95 +4.93 +0.62 +4.72 +2.35 +2.04 +4.21 +3.27
3.90 3.39 0.96 3.13 0.40 0.87 0.44 0.37 0.74 3.64
PDV
No.
Age (y)/ gender
+3.90 +4.43 +0.90 +2.98 +0.43 +0.32 +0.39 +0.52 +0.51 +3.37
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26/M 40/F 23/F 17/M 40/M 50/M
PSV
PDV
2.27 3.16 4.87 1.23 3.48 4.25 2.91 2.39 3.85 3.99
+2.07 +2.61 +3.09 +1.23 +2.44 +2.36 +2.75 +2.78 +3.38 +2.10
PDV = peak diastolic velocity, PSV = peak systolic velocity, ‘‘–” sign = craniocaudal flow, ‘‘+” sign = caudocranial flow.
(p < 0.05). Peak CSF velocities were <5 cm/s in all controls; but in 4 out of 10 patients with hydrocephalus, velocities were >6 cm/s, which suggested hyperdynamic flow through the aqueduct (Table 4). The pre-shunt study group demonstrated higher values of mean flow (range 0.00 cm3/s to 0.44 cm3/s) (Table 4). In 7/10 patients, the mean CSF flow was >0.02 cm3/s. In these 7 patients, the mean flow rate was reduced post-shunt, but the difference was not statistically significant. 4. Discussion The non-invasive evaluation of CSF flow using MRI has evolved from visual qualitative techniques to a quantitative technique using cine phase-contrast CSF velocity MR imaging. Many authors have evaluated CSF flow dynamics across the aqueduct of Sylvius in healthy individuals and in patients with known or suspected CSF circulation disorders.1,4,7–13 Based on the clinical significance of detected CSF abnormalities, various authors have predicted which patients with hydrocephalus are likely to improve following CSF diversion.8,10–14,16–18 In 1991 Bradley et al. reported a highly significant association between a prominent CSF flow void in the cerebral aqueduct and a favorable response to surgery (CSF diversion).14 Our experience was similar. However, in 1996, Bradley et al. found no statistically significant association between flow void and response to CSF diversion.17 The measurement of flow void is highly dependent on acquisition parameters as well as the technical characteristics of MRI systems (e.g. gradient strength). In addition; evaluation of
the flow void is subjective, possibly rendering it a less sensitive predictor. In our study, the PSVs and PDVs, mean velocity and aqueductal CSF stroke volume demonstrated marked variation between individuals in both the study and the control groups. There was no correlation with the age or sex of the individuals. These findings are consistent with previous reports.6,9,15,19 In the patients with hydrocephalus, the aqueduct area was significantly greater than in the controls, and post-shunt values were not significantly different from those of the control group. These results are similar to Henry-Feugeas et al.20 and Bradley et al.19 In two of our patients, the aqueduct completely collapsed postoperatively. This made placement of the ROI over the aqueduct difficult, and subsequent evaluation of the quantitative flow parameters became subject to error. The resistance to CSF flow through the aqueduct is inversely proportional to the fourth power of its radius; therefore, small changes in the size of the aqueduct cause large changes in CSF flow. The aqueductal CSF stroke volume is an average volume of CSF moving in a craniocaudal direction during systole and caudocranial direction during diastole. In 1996 Bradley et al. reported that patients with stroke volumes greater than 42 lL responded to shunting while 50% of the patients with stroke volume less than 42 lL did not respond.17 In our study group, 6 patients had high stroke volumes (>50 lL) and the other 4 had stroke volume values that fell in the ‘‘normal” range. After shunt surgery, the stroke volumes reduced significantly (0.6–48.77 lL), which indicated a functional VP shunt. The difference between stroke volumes in patients and controls was statistically significant, and so was the reduction in stroke volumes post CSF diversion. In our study, a cut-off value of P50 lL of the aqueductal CSF stroke volume defined hyperdynamicity of CSF flow, whereas values between 35 lL and 50 lL constituted the intermediate or the ‘‘grey” zone. Our observation of clinical improvement in 5 out of 6 patients with high stroke volumes corroborates with previous reports.21 However; in our study, the difference was not statistically significant (p = 0.066). Our observation of a wide range of peak CSF velocities through the aqueduct is in accordance with previous reports.6,9,11,15,19 Although peak velocity was not a very good parameter for differentiating patients with hydrocephalus from normal individuals, amplitudes greater than 6 cm/s suggested communicating hydrocephalus with hyperdynamic flow. After shunt surgery, peak velocity was reduced in 9 out of 10 patients. We observed greater CSF velocities in craniocaudal direction (in systole) than caudocranial direction (diastole) in both the study and control groups. In addition, the amplitudes of systolic velocity peaks were greater than amplitudes of diastolic velocity peaks in 9/ 10 controls and 7/10 cases of hydrocephalus. Similar observations have been reported previously.6,19
Table 4 Mean velocity (cm/s) and mean flow (cm3/s) of pre-shunt and post-shunt cerebrospinal fluid (Craniocaudal flow is negative by convention) Patient
Controls Pre-shunt
No.
Age (y)/gender
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26 /M 40/F 23/F 17/M 40/M 50/M
Mean velocity 0.89 0.72 0.88 0.63 0.28 0.67 0.03 0.03 0.01 0.15
Post-shunt Mean flow 0.11 0.20 0.05 0.05 0.07 0.05 0.00 0.00 0.44 0.01
Mean velocity 0.16 0.17 0.06 0.15 0.02 0.21 0.06 0.07 0.02 0.27
Mean flow 0.04 0.01 0.00 0.01 0.00 0.00 0.00 0.00 0.00 0.02
No.
Age (y)/gender
1 2 3 4 5 6 7 8 9 10
26/M 23/M 45/M 21/F 26/M 40/F 23/F 17/M 40/M 50/M
Mean velocity 0.52 0.48 0.60 0.10 0.79 0.50 0.34 0.22 0.32 0.41
Mean flow 0.00 0.01 0.02 0.00 0.01 0.01 0.01 0.01 0.01 0.01
518
P. Abbey et al. / Journal of Clinical Neuroscience 16 (2009) 514–518
5. Conclusion In conclusion, the qualitative and quantitative assessment of CSF flow using phase-contrast MRI can provide information about various flow parameters in normal individuals and also demonstrate altered flow dynamics in patients with communicating hydrocephalus. Increased aqueductal CSF stroke volume in patients with hydrocephalus predicts the likelihood of clinical improvement post CSF diversion. Repeat evaluation after shunt surgery helps establish how well the shunt system is functioning. CSF flow parameters in patients with hydrocephalus post VP shunt are similar to those in healthy subjects.
References 1. Nitz WR, Bradley Jr WG, Watanabe AS, et al. Flow dynamics of cerebrospinal fluid: assessment with phase contrast velocity MR imaging performed with retrospective cardiac gating. Radiology 1992;183:395–405. 2. Levy LM, Di Chiro G. MR phase imaging and cerebrospinal fluid flow in the head and spine. Neuroradiology 1990;32:399–406. 3. Quencer RM, Post MJ, Hinks RS. Cine MR in the evaluation of normal and abnormal CSF flow: intracranial and intraspinal stiudies. Neuroradiology 1990;32:371–91. 4. Henry–Feugeas MC, Idy-Peretti I, Blanchet B, et al. Temporal and spatial assessment of normal cerebrospinal fluid dynamics with MR imaging. Magn Reson Imaging 1993;11:1107–18. 5. Bhadelia RA, Bogdan AR, Wolpaert SM. Analysis of cerebrospinal fluid flow wave forms with gated phase-contrast MR velocity measurements. Am J Neuroradiol 1995;16:389–400. 6. Bhadelia RA, Bogdan AR, Kaplan RF, et al. Cerebrospinal fluid pulsation amplitude and its quantitative relationship to cerebral blood flow pulsations: a phase-contrast MR flow imaging study. Neuroradiology 1997;39:258–64. 7. Parkkola RK, Komu MES, Aarimaa TM, et al. Cerebrospinal fluid in children with normal and dilated ventricles studied by MR imaging. Acta Radiol 2001;42:33–8.
8. Bradley Jr WG, Scalzo D, Queralt J, et al. Normal pressure hydrocephalus: evaluation with cerebrospinal fluid flow measurements at MR imaging. Radiology 1996;198:523–9. 9. Gideon P, Thomsen C, Stahlberg F, et al. Cerebrospinal fluid production and dynamics in normal aging: a MRI phasemapping study. Acta Neurol Scand 1994;89:362–6. 10. Jacobson EE, Fletcher DF, Morgan MK. Fluid dynamics of the cerebral aqueduct. Pediatr Neurosurg 1996;24:229–36. 11. Kim DS, Choi JU, Huh R, et al. Quantitative assessment of cerebrospinal fluid hydrodynamics using a phase-contrast cine MR image in hydrocephalus. Childs Nerv Syst 1999;15:461–7. 12. Schroeder HWS, Schweim C, Schweim KH, et al. Analysis of aqueductal cerebrospinal fluid flow after endoscopic aqueductoplasty by using cine phasecontrast magnetic resonance imaging. J Neurosurg 2000;93:237–44. 13. Parkkola RK, Komu MES, Kotilainen EM, et al. Cerebrospinal fluid flow in patients with dilated ventricles studied with MR imaging. Eur Radiol 2000;10:1442–6. 14. Bradley WG, Whitemore AR, Watanabe AS, et al. Association of deep white matter infarction with chronic communicating hydrocephalus: implications regarding the possible origin of normal pressure hydrocephalus. Am J Neuroradiol 1991;12:31–9. 15. Gideon P, Stahlberg F, Thomsen C, et al. Cerebrospinal fluid flow and production in patients with normal pressure hydrocephalus studied by MRI. Neuroradiology 1994;36:210–5. 16. Mascalchi M, Arnetoli G, Inzitari D, et al. Cine-MR imaging of aqueductal CSF flow in normal pressure hydrocephalus syndrome before and after CSF shunt. Acta Radiol 1993;34:586–92. 17. Bradley WG, Kortman KE, Burgoyne B. Flowing cerebrospinal fluid in normal and hydrocephalic states: appearance on MR images. Radiology 1996;159:611–6. 18. Barcena A, Mestre C, Canizal JM, et al. Idiopathic normal pressure hydrocephalus: analysis of factors related to cerebrospinal fluid dynamics determining functional prognosis. Acta Neurochir 1997;139: 933–41. 19. Bradley WG, Whitemore A, Jinkins JR, et al. Cerebrospinal fluid flow patterns in hydrocephalus: correlation of clinical and phantom studies using MR imaging. Radiology 1987;165:78–9. 20. Henry-Feugeas MC, Idy-Peretti I, Baledent O, et al. Cerebrospinal fluid flow waveforms: MR analysis in chronic adult hydrocephalus. Invest Radiology 2001;36:146–54. 21. Borgsen SE, Gjerris F, Sorensen SC. Cerebrospinal fluid conductance and compliance of the cranial spinal space in normal pressure hydrocephalus. Neurosurg 1979;51:521–5.