Ventricle wall movements and cerebrospinal fluid flow in hydrocephalus

Clinical article

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Object

The dynamics of fluid flow in normal pressure hydrocephalus (NPH) are poorly understood. Normally, CSF flows out of the brain through the ventricles. However, ventricular enlargement during NPH may be caused by CSF backflow into the brain through the ventricles. A previous study showed this reversal of flow; in the present study, the authors provide additional clinical data obtained in patients with NPH and supplement these data with computer simulations to better understand the CSF flow and ventricular wall displacement and emphasize its clinical implications.

Methods

Three NPH patients and 1 patient with aqueductal stenosis underwent cine phase-contrast MR imaging (cine MR imaging) for measurement of CSF flow and ventricle wall movement during the cardiac cycle. These data were compared to data previously obtained in 8 healthy volunteers.

The CSF flow measurements were obtained at the outlet of the aqueduct of Sylvius. Calculation of the ventricular wall movement was determined from the complete set of cine MR images obtained axially at the middle of the lateral ventricle. The data were obtained before and after CSF removal with a ventriculoperitoneal shunt with an adjustable valve. To supplement the clinical data, a computational model was used to predict the transmural pressure and flow.

Results

In healthy volunteers, net CSF aqueductal flow was 1.2 ml/minute in the craniocaudal direction. In patients with NPH, the net CSF flow was in the opposite direction—the caudocranial direction—before shunt placement. After shunting, the magnitude of the abnormal fluid flow decreased or reversed, with the flow resembling the normal flow patterns observed in healthy volunteers.

Conclusions

The authors' MR imaging–based measurements of the CSF flow direction and lateral ventricle volume size change and the results of computer modeling of fluid dynamics lead them to conclude that the directional pattern and magnitude of CSF flow in patients with NPH may be an indication of the disease state. This has practical implications for shunt design and understanding the mechanisms that produce hydrocephalus.

Abbreviations used in this paper: cine MR imaging = cine phase-contrast MR imaging; NPH = normal pressure hydrocephalus; VP = ventriculoperitoneal.

Article Information

Address correspondence to: Richard Penn, M.D., Department of Bioengineering, University of Illinois at Chicago, Science and Engineering Offices (SEO), Room 218 (M/C 063), 851 South Morgan Street, Chicago, Illinois 60607-7052. email: richardpenn@ameritech.net.

Please include this information when citing this paper: published online January 28, 2011; DOI: 10.3171/2010.12.JNS10926.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Schematic of the model highlighting areas of interest. Note that the normal pattern of CSF flow is from the third ventricle (3V) to the fourth ventricle (4V) and that this reverses in hydrocephalus. The obstruction to flow out of the subarachnoid space (SAS) to the venous sinus (vSinus) causes a reversal of the pressure gradient from the brain parenchyma to the lateral ventricles (LV), which in turn results in the flow direction change. The model predicts this reversal. The shunt reduces the gradient and brings the flow pattern back to normal. cAr = carotid artery; Ar = artery; AI = arteriole; Cp = capillary; V = vein; VI = venule. Superscript L and R refer to left and right, respectively. The thickness of the arrows indicates volume of flow and the relative size of the boxes indicate degree of wall displacement relative to the normal size.

  • View in gallery

    Computer simulation showing the pressure across the ventricle and brain parenchyma. The normal case (Frame A) shows a higher average brain pressure (solid line), which indicates flow from the brain to the ventricles. Frame B shows higher ventricular pressure (dashed line) due to hydrocephalus, which indicates flow reversal. Frame C shows the effect of fluid removal from the right ventricle and the reversal of pressure to normal.

  • View in gallery

    Computer simulation of CSF net flow in the normal and hydrocephalic brain. Net flow is from the parenchyma to the ventricles in the normal case (left); net flow is from the ventricles to the brain parenchyma in the hydrocephalic case (right).

References

1

Abbott NJ: Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology. Neurochem Int 45:5455522004

2

Chiang WWTakoudis CGLee SHWeis-McNulty AGlick RAlperin N: Relationship between ventricular morphology and aqueductal cerebrospinal fluid flow in healthy and communicating hydrocephalus. Invest Radiol 44:1921992009

3

Czosnyka MCzosnyka ZMomjian SPickard JD: Cerebrospinal fluid dynamics. Physiol Meas 25:R51R762004

4

Czosnyka ZHCieslicki KCzosnyka MPickard JD: Hydrocephalus shunts and waves of intracranial pressure. Med Biol Eng Comput 43:71772005

5

Davson HSegal MB: Physiology of the CSF and Blood-Brain Barriers Boca Raton, FLCRC Press1996. 822

6

Egnor MZheng LRosiello AGutman FDavis R: A model of pulsations in communicating hydrocephalus. Pediatr Neurosurg 36:2813032002

7

Eide PK: Demonstration of uneven distribution of intracranial pulsatility in hydrocephalus patients. Clinical article. J Neurosurg 109:9129172008

8

Greitz DFranck ANordell B: On the pulsatile nature of intracranial and spinal CSF-circulation demonstrated by MR imaging. Acta Radiol 34:3213281993

9

Huang TYChung HWChen MYGiiang LHChin SCLee CS: Supratentorial cerebrospinal fluid production rate in healthy adults: quantification with two-dimensional cine phase-contrast MR imaging with high temporal and spatial resolution. Radiology 233:6036082004

10

Kim DSChoi JUHuh RYun PHKim DI: Quantitative assessment of cerebrospinal fluid hydrodynamics using a phasecontrast cine MR image in hydrocephalus. Childs Nerv Syst 15:4614671999

11

Levine DN: Intracranial pressure and ventricular expansion in hydrocephalus: have we been asking the wrong question?. J Neurol Sci 269:1112008

12

Linninger AASweetman BPenn R: Normal and hydrocephalic brain dynamics: the role of reduced cerebrospinal fluid reabsorption in ventricular enlargement. Ann Biomed Eng 37:143414472009

13

Linninger AATsakiris CZhu DCXenos MRoycewicz PDanziger Z: Pulsatile cerebrospinal fluid dynamics in the human brain. IEEE Trans Biomed Eng 52:5575652005

14

Linninger AAXenos MSweetman BPonkshe SGuo XPenn R: A mathematical model of blood, cerebrospinal fluid and brain dynamics. J Math Biol 59:7297592009

15

Peña ABolton MDWhitehouse HPickard JD: Effects of brain ventricular shape on periventricular biomechanics: a finite-element analysis. Neurosurgery 45:1071181999

16

Penn RDLinninger A: The physics of hydrocephalus. Pediatr Neurosurg 45:1611742009

17

Taylor ZMiller K: Reassessment of brain elasticity for analysis of biomechanisms of hydrocephalus. J Biomech 37:126312692004

18

Wilkie KPDrapaca CSSivaloganathan S: A theoretical study of the effect of intraventricular pulsations on the pathogenesis of hydrocephalus. Appl Math Comput 215:318131912010

19

Zhu DCXenos MLinninger AAPenn RD: Dynamics of lateral ventricle and cerebrospinal fluid in normal and hydrocephalic brains. J Magn Reson Imaging 24:7567702006

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