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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 46  |  Issue : 2  |  Page : 121-132

Cerebrospinal fluid flowmetry using phase-contrast MRI technique and its clinical applications


Radiodiagnosis Department, Tanta University Hospitals, Egypt

Date of Submission01-Jun-2017
Date of Acceptance09-Jul-2018
Date of Web Publication31-Oct-2018

Correspondence Address:
Hend G Elsafty
Radio-diagnosis and Medical Imaging Department, Faculty of Medicine, Tanta University, El Gharbia, Tanta, El Nahass Street
Egypt
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DOI: 10.4103/tmj.tmj_55_17

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  Abstract 


Background and aim and aim Cine phase-contrast (PC) MRI is a useful noninvasive imaging technique in evaluating the dynamics of cerebrospinal fluid (CSF) in the evaluation, follow-up, surgical decision, and postoperative survey of certain disease processes, such as normal pressure hydrocephalus, aqueduct stenosis (AS), postendoscopic third ventriculostomy, and arachnoid cysts cases. The aim of this study was to determine the value of cardiac-gated cine-PC-MRI in characterizing CSF flow in patients with CSF flow disorders.
Patients and methods The study included 30 patients with 10 persons as the control group and 20 patients who were suspected to have CSF flow abnormalities. Two imaging techniques were applied: the axial plane for flow quantification and the sagittal plane for a qualitative assessment.
Results Among the 30 patients, quantitative analysis revealed the mean value to be 22 μl as the average aqueductal stroke volume in the control group. In the normal pressure hydrocephalus group, systolic velocities as well as stroke volume values were higher than those of the controls. In the AS group, lack of significant aqueductal CSF flow was noticeable. Both peak systolic and diastolic velocities were found to be statistically significantly lower in patients with AS than in the control group. In arachnoid cyst cases, CSF flow study with cine PC-MRI enables visualization of flow communication between cysts and neighboring CSF compartments. Two cases were assigned as communicating cysts and four cases were noncommunicating.
Conclusion Assessment of CSF flow indicates the potentials of using PC-MRI adjunct to routine MR for the clinical study of CSF-related diseases.

Keywords: csf flow


How to cite this article:
Elsafty HG, ELAggan AM, Yousef MA, Badawy ME. Cerebrospinal fluid flowmetry using phase-contrast MRI technique and its clinical applications. Tanta Med J 2018;46:121-32

How to cite this URL:
Elsafty HG, ELAggan AM, Yousef MA, Badawy ME. Cerebrospinal fluid flowmetry using phase-contrast MRI technique and its clinical applications. Tanta Med J [serial online] 2018 [cited 2018 Nov 21];46:121-32. Available from: http://www.tdj.eg.net/text.asp?2018/46/2/121/244688




  Introduction Top


During the last two decades, flow-sensitive MRI techniques have been increasingly applied to assess quantitatively and qualitatively the cerebrospinal fluid (CSF) flow dynamics [1].

CSF flow MRI can be used to discriminate between communicating hydrocephalus and noncommunicating hydrocephalus, to localize the level of obstruction in obstructive hydrocephalus, to determine whether arachnoid cysts communicate with the subarachnoid space, to differentiate between arachnoid cysts and subarachnoid space, to discriminate between syringomyelia and cystic myelomalacia, and to evaluate the flow patterns of posterior fossa cystic malformations [2].

This imaging method can also provide significant information in preoperative evaluation of  Chiari malformation More Details type 1 and normal pressure hydrocephalus (NPH) and postoperative follow-up of patients with neuroendoscopic third ventriculostomy and ventriculoperitoneal shunt [3].

The absorption of the CSF is a dual process. It is chiefly a rapid drainage through the arachnoid villi into the great dural sinuses, but it also escapes slowly into the true lymphatic vessels by way of an abundant but indirect perineural (ophthalmic, optic and vagal nerves) course and via the capillary bed of the central nervous system. Two components can be distinguished in CSF circulation: (i) bulk flow (circulation) and (ii) pulsatile flow (back and forth motion). In bulk flow theory, CSF is produced by the choroid plexus and is absorbed by arachnoid granulations [4].

The force, which provides CSF movement from the ventricular system to arachnoid granulation and CSF absorption, is caused by a hydrostatic pressure gradient between the site of its formation (slightly high pressure) and its site of absorption (slightly low pressure). In pulsatile flow theory, movement of the CSF is pulsatile and results from pulsations related to the cardiac cycle of the choroid plexus and the subarachnoid portion of the cerebral arteries. Since very little CSF water truly circulates through the subarachnoid space, pulsatile flow, rather than bulk flow, can be measured and demonstrated by PC-MRI [4].


  Patients and methods Top


Patients and control group

The study was carried out on 20 patients (group I) suspected to have CSF flow abnormalities based on clinical symptoms and conventional MRI findings and 10 normal control persons group II with the same age and sex as the patients group I and it was carried out on an TOSHIPA MRI machine 1.5 t on educational new Hospital Tanta University.

Exclusion criteria

Patients with complex febrile seizures, neurologic diseases, cerebrovascular risk factors, and using any anticonvulsive medications in addition to cardiac patients with arrhythmia, in addition to routine MRI contraindication as pacemaker, claustrophobic patients, and patients with intracranial metal clips and neurostimulators were excluded from the study.

Inclusion criteria

Patients suspected to have CSF flow abnormalities based on clinical symptoms and conventional MRI findings such as NPH, aqueductal stenosis (AS), Chiari malformation type 1, syringomyelia, and arachnoid cysts.

All patients were evaluated as follows:
  1. Complete history taking including present and past history.
  2. Written informed consent was obtained from all patients after full explanation of the technique and how the machine work.
  3. There was a code number for each patient’s file that includes all investigations.
  4. Privacy of all patients’ data was guaranteed.
  5. Any unexpected risks that appeared during the course of the research were cleared to the participants and the ethics committee on time.
  6. MRI examinations were performed with a 1.5-T MR unit; imaging was carried out using standard head coils, in neutral supine position and without any case preparation. Routine conventional MRI sequences including, axial T1, T2, and FLAIR, sagittal T2 and coronal T2 were done. The measurement parameters of T2 were as follows: TR 5000, TE 105, NEX 2, FA1/10°; FOV 240, matrix 224×384.
    • Mid-sagittal steady-state free precession sequence with thin cuts for better assessment of CSF flow void sign along the aqueduct of Sylvius.
  7. In all cases, cardiac gating was performed with MR-compatible electrodes. A localizer was placed on the cerebral aqueduct, perpendicular to the ampullar region of the aqueduct on sagittal T2-weighted images or SSPS sequence.
  8. Two-dimensional cine phase-contrast MRI (2D cine PC-MRI) which is cardiac gated for the detection of CSF flow during systole and diastole with the following imaging parameters were as follows: TR=25, TE=4.3, flip angle=10°, number of acquisitions=2, field of view: 180 mm, matrix: 128×512, scan thickness: 1 mm, phase encoding velocity encoding (VENC): 5–20 cm/s measurement time according to patient heart rate was ∼2.25 min.


Different protocols of examination were done
  1. CSF flow properties were analyzed at the level of the aqueduct of Sylvius in most of the patients with the exception of those patients who underwent endoscopic third ventriculostomy (ETV), where we analyzed the CSF flow at the level of the third ventricle floor fenestration.
  2. In arachnoid cyst cases, we detect the communication with the subarachnoid spaces by noting the jet flow between the cyst and the cisterns on cine PC-MR and SSPS sequence.
  3. Two imaging techniques were applied: one in the axial plane with through-plane VENC in the caudocranial direction for flow quantification, and one in the sagittal plane within-plane VENC in the craniocaudal direction for a qualitative assessment.
  4. VENC (=5–20 cm/s) determines the highest and lowest detectable VENC by a PC sequence and it should exceed the expected maximum velocity within the selected ROI to avoid aliasing. Usually low VENC (3–5) selected in cases of arachnoid cysts and AS, high VENC (15–20) selected in NPH and ETV cases.
  5. CSF flow quantification was performed on those phase images using the region-of interest (ROI) measurements and a CSF flow wave form was generated. A circular ROI was drawn so to include those pixels that reflected the CSF flow signals of the cerebral aqueduct on the phase images.
  6. The ROI was placed in the aqueduct shown on a magnified image. In patients with AS, the ROI was placed within the visualized area of CSF flow representing the present aqueductal lumen and determined as an area of phase change with respect to the background.
  7. On the CSF flow waveform, the time of the cardiac cycle was plotted on the x axis and the velocity on the y axis. Each curve has a corresponding table showing the CSF velocity and flow values for each time frame.


Postprocessing calculation including the following:

  1. Peak systolic velocity (cm/s), highest CSF velocity of the obtained measurement during the systole.
  2. End diastolic velocity (cm/s), highest CSF velocity of the obtained measurement during the diastole.
  3. Mean (average) velocity (cm/s) during both systole and diastole.
  4. Flow rate (ml/min)=ROI (cm2)×mean velocity.
  5. Stroke volume (μl) defined the mean volume of CSF passing the aqueduct during the systole=mean flow×CSF duration during the systole.


Statistical analysis

  1. Data were processed using the Statistical Package for the Social Sciences program (SPSS) version 21 of IBM (USA).
  2. Qualitative variables were presented as number and percentage and χ2-test was used for analysis and when not appropriate, Fischer’s exact test was used.
  3. Quantitative variables were presented as mean and SD, also median and interquartile range because the data are nonparametric. As a result, Mann–Whitney U and Kruskal–Wallis H-tests were used for the analysis.
  4. Level of significance was adopted at a P value of less than 0.05.



  Results Top


Among the 30 patients included in the present study, men were more than women representing 57 and 43%, respectively. The age ranged between 18 months and 67 years ([Table 1]).
Table 1 Sociodemographic characteristics of the studied patients

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Cine PC-MRI was used to study the aqueductal CSF flow in 10 control group (six men and four women); their age averaged 22.75 years [SD 19.53, range: 56.4 (1.6–68 years)], seven persons (NPH group) with symptomatic ventriculomegaly (one men and six women). Their age averaged 58.29 years [SD 5.79, range: 17 (50–67) years], four patients with AS (two men and two women). Their age averaged 27.5 years [SD 9.57 months, range 22 (17–39)], three persons (three men) underwent ETV as a postoperative follow-up to assess the patency and the function of the third ventriculostomy soma. Their age averaged 35.3 years [SD 28.68, range: 57 (5–62)], six persons (five men and one women) with arachnoid cyst by routine MRI. Their age averaged 22.67 years [SD 16.17 years, range 32 (8–40)].

The values of the parameters of aqueductal CSF flow are summarized in [Table 2] with the mean values of peak velocities and volumetric flow parameters in NPH patients were found to be high but not significantly higher compared with the normal control group and atrophy patients (nonsignificant, P=0.37). In the remaining three patients, the velocity and volumetric flow parameters were nonelevated/nonreduced and did not differ significantly between the normal control group.
Table 2 Comparison between control and normal pressure hydrocephalus groups regarding PSV, EDV, mean velocity, mean systolic flow, systolic duration, and stroke volume

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In the four patients of the AS group, no flow was detected in the aqueduct by cine PC-MRI and mean values of peak velocities were found significantly lower compared with the normal control group ([Table 3]).
Table 3 Comparison between control and aqueduct stenosis groups regarding PSV, EDV, and mean velocity

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Mean values of stroke volume in patients post-ETV were found significantly higher compared with the normal control (P=0.01) which matched with a well-functioning stoma ([Table 4]).
Table 4 Comparison between control and endoscopic third ventriculostomy groups regarding PSV, EDV, mean velocity, and stroke volume

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Characters of cerebrospinal fluid flow in the arachnoid cyst group

Cine PC-MRI was used to study the CSF flow in six persons (five men and one women) with the arachnoid cyst diagnosed by routine MRI; four patients were assigned as having noncommunicating arachnoid cyst and two patients were found to be communicating AC which was confirmed by surgery ([Table 5]).
Table 5 Clinical and MRI findings of the arachnoid cyst group

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Cases

Case 1

[Figure 1] 22-year old male normal volunteer, shows normal conventional MRI. A, coronal T2, B axial T2, C sagittal T2.
Figure 1 Conventional MRI.

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[Figure 2] shows CSF flow study.

  • A1. ROI selected through the aqueduct.
  • A2. Peak velocity curve.
  • A3. Peak velocity values throughout the cardiac cycle.
  • B1. ROI selected through the aqueduct.
  • B2. Mean velocity curve.
  • B3. Mean velocity values throughout the cardiac cycle.
  • C1. ROI selected through the aqueduct.
  • C2. Mean flow curve.
  • C3. Mean flow values throughout the cardiac cycle.
Figure 2 Cerebrospinal fluid flow study.

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Quantitative assessment by cerebrospinal fluid flow parameters

  • Peak systolic velocity=4.8 cm/s.
  • End diastolic velocity=3.8 cm/s.
  • Mean velocity measures=3.1 cm/s.
  • Systolic duration=360 ms.
  • Estimated absolute stroke volume=18 μl.


Case note: normal CSF velocities and absolute stroke volume.

Conclusion

Normal conventional MRI and CSF flowmetry findings.

Case 2

[Figure 3] A 54-year woman who presented with dementia, drowsiness, and gait disturbance: A. coronal T2, B. axial T2, C. axial FLAIR, D. sagittal T2. Dilated lateral and third ventricle with normal fourth ventricle with periventricular hyperintensities denoting gliosis.
Figure 3 Conventional MRI.

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[Figure 4] CSF flow study.
Figure 4 Cerebrospinal fluid flow study.

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Quantitative assessment by cerebrospinal fluid flow parameters

  • Peak systolic velocity=1.2 cm/s.
  • End diastolic velocity=1 cm/s.
  • Mean velocity measures=1 cm/s.
  • Systolic duration=350 ms.
  • Estimated absolute stroke=5 μl.


Case note: low CSF velocities and absolute stroke volume with no flow void detected through the aqueduct.

Conclusion

The findings are impressive of a relatively hypodynamic CSF circulation in view of routine MRI findings;, the diagnosis of atrophy is most likely.

Case 3

[Figure 5] A male patient aged 67 years who presented with dementia, gait disturbance, and incontinence: A sagittal T2, B axial T2, D sagittal constructing imaging in the steady-state (CISS) sequence. Dilated ventricular system out of proportion of peripheral atrophic brain changes with aqueductal flow void detected through the aqueduct of Sylvius in CISS sequence is shown.
Figure 5 (a) Sagittal constructing imaging in the steady-state and (b) axial T2.

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[Figure 6] the CSF flow study.
Figure 6 Cerebrospinal fluid flow study.

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Quantitative assessment by cerebrospinal fluid flow parameters

  • Peak systolic velocity=8.8 cm/s.
  • End diastolic velocity=5 cm/s.
  • Mean velocity measures=1.07 cm/s.
  • Systolic duration=400 ms.
  • Estimated absolute stroke volume=156 μl.


Case note: markedly elevated CSF velocities and absolute stroke volume with evident flow void detected through the aqueduct.

Conclusion

The findings are impressive for hyperdynamic CSF circulation, in view of patient history and routine MRI findings; diagnosis of NPH is most likely.

Case 4

[Figure 7] A 23 year women who presented with headache, visual impairment, and exophthalmos: A axial T2, B sagittal T2, C coronal T2, D sagittal SSPS sequence. Moderate supratentorial hydrocephalus with evidence of AS by adhesion in the sagittal SSPS sequence is shown.
Figure 7 (a) Axial T2, (b) sagittal T2, (c) coronal T2, and (d) sagittal three-dimensional steady-state free precession.

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[Figure 8] shows the CSF flow study.
Figure 8 Cerebrospinal fluid flow study.

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Quantitative assessment by cerebrospinal fluid flow parameters

  • Peak systolic velocity=0.6 cm/s.
  • End diastolic velocity=0.3 cm/s.
  • Mean velocity measures=0.22 cm/s.


Case note: low CSF velocities distal to the obstruction with reverberated appearance of CSF velocity time curve due to turbulence of the flow proximal to the obstruction.

Conclusion

Supratentorial hydrocephalus with AS.


  Discussion Top


PC-MRI and three-dimensional CISS sequence have been increasingly used during the last decade for evaluating cranial and spinal CSF flow [5].

Thirty patients were included in our study with different varieties including 10 normal controls, seven patients of the NPH group, four patients with AS, three patients who underwent ETV as a postoperative follow-up to assess the patency and the function of the third ventriculostomy soma, and six patients with arachnoid cysts.

Qualitative assessment of cerebrospinal fluid flow (sagittal phase contrast images)

In this study, the normal aqueductal flow was homogeneous with sinusoidal bidirectional velocity. So the results of our study support the current opinion of CSF circulation that was indeed described by Bhadelia that the cardiac cycle-related cerebral blood volume variations produce bidirectional oscillatory movement of the CSF within the craniospinal axis. During systole, the net inflow of blood increases the intracranial volume and induces craniocaudal (systolic) CSF flow. During diastole, the net outflow of blood decreases the intracranial volume and promotes caudocranial (diastolic) CSF flow [6].

Quantitative assessment of cerebrospinal fluid flow (axial phase contrast images)

In our study, in the control group, the peak systolic velocity at the level of the aqueduct was around 4.62 (±0.7) cm/s; the mean flow was around 0.097 (±0.059) ml/s. The velocity and flow parameters are striking as reported by several investigators. Also we obtained a mean value of 22.2 (±9.0) μl for aqueductal systolic volume, which is very close to the study reported by Schroder who reported a stroke volume of 28 μl in normal individuals [7].

In NPH patients

We reported obvious elevation of the mean systolic flow as well as the absolute stroke volume in comparison to the control group, indicating hyperdynamic circulation. The stroke volume was found higher with a mean value of 46.7 (±52.6) μl compared with 22.2(±9.0) μl in the normal control group; however, there were no evident statistical significance (P=0.37). Our results were not compatible with previous studies done on NPH patients, by Kahlon and colleagues which reported a statistically significant difference between the NPH group and the control group as his study was performed on a larger number of patients. We also observed that those patients with the hyperdynamic CSF flow responded well to shunt surgery by clinical improvement, which correlate with the study performed by Bradley, who reported that the patients who responded well to shunting for NPH have at least twice the aqueductal stroke volume of healthy elderly patients [8],[9].

Also our study included the differentiation between NPH patients and atrophy group as both conditions are characterized by ventriculomegaly and the clinical picture is greatly overlapping, here comes the application of the CSF flow studies. In our study, we found patients to have markedly lower stroke volume in comparison to the normal control group, indicating hypodynamic circulation in patients with atrophy which is compatible with the study performed by Abdallah et al. [10], who reported that In cerebral atrophy, blood flow to the brain is decreased; we found markedly lower systolic peak velocity, systolic mean velocity, and stroke volume values in comparison to healthy volunteers indicating a hypodynamic CSF circulation.

We studied four patients with AS with mean peak systolic velocities of around 1.1 (±0.62 cm/s) and peak diastolic velocities of around 1.63 (±2.03 cm/s) which were found to be lower than the normal control group. These findings are compatible with a study performed on 16 patients by Kim et al. [11]. In the 16 cases, the aqueductal CSF flow maximum systolic velocity was less than 1 cm/s.

In patients post-ETV, our results showed two patients with clinical improvement and reduction in venticulomegaly after the operation with overall flow amplitude and stroke volume across the ventriculostomy was found to be high, with a mean value of around 71.0 (±18.5), which is found to be significantly higher (P=0.048) compared with the normal aqueductal CSF flow in the control group, and only one patient was found to be with poorly functioning stoma with clinical deterioration after the operation and relatively low overall flow amplitude compared with the patients with well-functioning stoma; these results were found to be matched with the study performed by Tisell et al. [12], who concluded a good correlation between clinical improvement and the overall flow volume and stroke volume. He also reported that when the stroke volume obtained in the ventriculostomy is high, the clinical outcome is usually good.

Qualitative assessment of the cerebrospinal fluid flow in patients with arachnoid cyst

We study the CSF flow in six persons with arachnoid cyst previously known by routine MRI. Two patients were found to be communicating AC by noting the jet flow between the cyst and the cisterns on cine PC-MR and SSPS sequence and four patients were assigned as noncommunicating arachnoid cyst by observing no alteration in signal intensity within the cyst, the results were confirmed by surgery.

The determination of whether the arachnoid cyst is communicating or not to the CSF spaces is important in the preoperative evaluation and for the proper management as the communicating cyst is better managed by cyst membrane fenestration into the subarachnoid spaces/cisterns while the noncommunicating one was better managed by cyst peritoneal shunt as mentioned in the study by Hoffmann et al. [13].

Conclusion

Assessments of CSF flow indicate the potentials of using PC imaging for quantitative and qualitative CSF flow analysis. It is a useful adjunct to routine MR for the clinical study of CSF-related diseases as well as for preoperative and postoperative follow-up, and as an aid for differential diagnosis in certain conditions.

Further large studies are recommended on a large number of patients using cine PC-MRI on different types of CSF disorders to evaluate its value in the diagnosis of these wide groups of diseases.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Yildiz H, Yazici Z, Hakyemez B et al. Evaluation of CSF flow patterns of posterior fossa cyst malformations using CSF flow MR imaging. Neuroradiology 2006; 48:595–605.  Back to cited text no. 1
    
2.
Bradley WG, Whittemore AR, Kortman KE et al. Marked cerebrospinal fluid void: indicator of successful shunt in patients with suspected normal-pressure hydrocephalus. Radiology 1991; 178:459–466.  Back to cited text no. 2
    
3.
Ng SE, Low AM, Tang KK et al. Idiopathic normal pressure hydrocephalus: correlating magnetic resonance imaging biomarkers with clinical response. Ann Acad Med Singapore 2009; 38:803–808.  Back to cited text no. 3
    
4.
Barkhof F, Kouwenhoven M, Scheltens P et al. Phase-contrast cine MR imaging of normal aqueductal CSF flow. Effect of aging and relation to CSF void on modulus MR. Acta Radiol 1994; 35:123–130.  Back to cited text no. 4
    
5.
Rieger A, Rainov G, Brucke M et al. Endoscopic third ventriculostomy is the treatment of choice for obstructive hydrocephalus due to pediatric pineal tumors. Minim Invasive Neurosurg 2000; 43:83–86.  Back to cited text no. 5
    
6.
Nitz WR, Bradley WG Jr, Wantanabe 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.  Back to cited text no. 6
    
7.
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; 39:258–264.  Back to cited text no. 7
    
8.
Levy LM, Di Chiro G. MR phase imaging and cerebrospinal fluid flow in the head and spine. Neuroradiology 1992; 32:399406.  Back to cited text no. 8
    
9.
Kahlon B, Annertz M, Ståhlberg F, Rehncrona S. Is aqueductal stroke volume, measured with cine phase-contrast magnetic resonance imaging scans useful in predicting outcome of shunt surgery in suspected normal pressure hydrocephalus? Neurosurgery 2007; 60:124–129.  Back to cited text no. 9
    
10.
Abdallah AEA, Shabaan MH, Hassan MA, Yassin AN. Giza/EG CNS, Neuroradiology brain, MR, MR-functional imaging, comparative studies, cerebrospinal fluid ECR 10, 2015. 1594/C-0117.  Back to cited text no. 10
    
11.
Kim DS, Choi JU, Yun PH, Kim DI. Quantitative assessment of cerebrospinal fluid hydrodynamics using a phase contrast cine MR image in hydrocephalus. Childs Nerv Syst 1999; 15:461–467.  Back to cited text no. 11
    
12.
Tisell M, Almstrom O, Stephensen H et al. How effective is endoscopic third ventriculostomy in treating adult hydrocephalus caused by primary aqueductal stenosis. Neurosurgery 2000; 46:104–111.  Back to cited text no. 12
    
13.
Hoffmann KT, Hosten N, Meyer BU et al. CSF flow studies of intracranial cysts and cyst-like lesions achieved using reversed fast imaging with steady-state precession MR sequences. Am J Neuroradiol 2000; 21:493–502.  Back to cited text no. 13
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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