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A mathematical model of blood, cerebrospinal fluid and brain dynamics

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Abstract

Using first principles of fluid and solid mechanics a comprehensive model of human intracranial dynamics is proposed. Blood, cerebrospinal fluid (CSF) and brain parenchyma as well as the spinal canal are included. The compartmental model predicts intracranial pressure gradients, blood and CSF flows and displacements in normal and pathological conditions like communicating hydrocephalus. The system of differential equations of first principles conservation balances is discretized and solved numerically. Fluid–solid interactions of the brain parenchyma with cerebral blood and CSF are calculated. The model provides the transitions from normal dynamics to the diseased state during the onset of communicating hydrocephalus. Predicted results were compared with physiological data from Cine phase-contrast magnetic resonance imaging to verify the dynamic model. Bolus injections into the CSF are simulated in the model and found to agree with clinical measurements.

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Abbreviations

cAr:

Carotid artery

Ar:

Arteries

Al:

Arterioles

Cp:

Capillaries

Vl:

Veinules

V:

Veins

vSinus:

Venous sinus

Lv:

Lateral ventricle

3V:

Third ventricle

4V:

Fourth ventricle

SAS:

Cranial subarachnoid space

sp.canal:

Spinal subarachnoid space

br:

Brain

exf:

Extracellular fluid

xxL,R :

Signifying two equations, one for the left brain hemisphere and one for the right brain hemisphere

xxR :

Right compartment

xxL :

Left compartment

\({{f}_{xx_{\rm in}}}\) :

Flow into the compartment

\({{f}_{xx_{\rm out}}}\) :

Flow out of the compartment

References

  • Baledent O, Henry-Feugeas MC, Idy-Peretti I (2001) Cerebrospinal fluid dynamics and relation with blood flow: a magnetic resonance study with semiautomated cerebrospinal fluid segmentation. Invest Radiol 36: 368

    Article  Google Scholar 

  • Bering EA (1962) Circulation of the cerebrospinal fluid. J Neurosurg 19: 405

    Article  Google Scholar 

  • Bertram CD, Brodbelt AR, Stoodley MA (2005) The origins of syringomyelia: numerical models of fluid/structure interactions in the spinal cord. J Biomed Eng 127: 1099

    Google Scholar 

  • Biot MA (1941) General theory of three-dimensional consolidation. J Appl Phys 12: 155

    Article  Google Scholar 

  • Biot MA (1955) Theory of elasticity and consolidation for a porous anisotropic solid. J Appl Phys 26(2): 182

    Article  MATH  MathSciNet  Google Scholar 

  • Brown P, Davies S, Speake T, Millar I (2004) Molecular mechanisms of cerebrospinal fluid production. Neuroscience 129: 957

    Article  Google Scholar 

  • Czosnyka Z, Czosnyka M, Richards HK, Pickard JD (2002) Laboratory testing of hydrocephalus shunts–Conclusion of the UK shunt evaluation programme. Acta Neurochir 144(6): 525

    Article  Google Scholar 

  • Czosnyka M, Czosnyka Z, Momjian S, Pickard JD (2004) Cerebrospinal fluid dynamics. Physiol Meas 25(5): R51

    Article  Google Scholar 

  • Czosnyka Z, Cieslicki K, Czosnyka M, Pickard JD (2005) Hydrocephalus shunts and waves of intracranial pressure. Med Biol Eng Comput 43(1): 71

    Article  Google Scholar 

  • Boor C (2001) A Practical guide to splines. Springer, New York

    MATH  Google Scholar 

  • DelBigio MR, Bruni JE (1988) Changes in periventricular vasculature of rabbit brain following induction of hydrocephalus and after shunting. J Neurosurg 69: 115

    Article  Google Scholar 

  • Dumoulin CL, Souza SP, Walker MF, Yoshitome E (1988) Time-resolved magnetic resonance angiography. Magn Reson Med 6(3): 275

    Article  Google Scholar 

  • Eklund A, Smielewski P, Chambers I, Alperin N, Malm J, Czosnyka M, Marmarou A (2007) Assessment of cerebrospinal fluid outflow resistance. Med Biol Eng Comput 45: 719

    Article  Google Scholar 

  • Fishman RA (1980) Cerebrospinal fluid in disease of the nervous system. W.B. Saunders Company, Philadelphia, pp 63–140

    Google Scholar 

  • Gjerris F, Borgensen SE (1992) Pathophysiology of cerebrospinal fluid circulation. In: Crockard A, Hayward A, Hoff J (eds) Neurosurgery: the scientific basis of clinical practice. Blackwell Scientific, Cambridge, pp 147–168

    Google Scholar 

  • Gosling RG, King DH (1974) Arterial assessment by Doppler-shift ultrasound. Proc R Soc Med 67: 447

    Google Scholar 

  • Greitz D, Hannerz J, Rahn T, Bolander H, Ericsson A (1994) MR imaging of cerebrospinal fluid dynamics in health and disease. On the vascular pathogenesis of communicating hydrocephalus and benign intracranial hypertension. Acta Radiol 35(3): 204

    Google Scholar 

  • Hakim S, Venegas JG, Burton JD (1976) The physics of the cranial cavity, hydrocephalus and normal pressure hydrocephalus: mechanical interpretation and mathematical model. Surg Neurol 5: 187

    Google Scholar 

  • Kaczmarek M, Subramaniam RP, Neff SR (1997) The hydromechanics of hydrocephalus: Steady-state solutions for cylindrical geometry. Bull Math Biol 59(2): 295

    Article  MATH  Google Scholar 

  • Kim J, Thacker NA, Bromiley PA, Jackson A (2007) Prediction of the jugular venous waveform using a model of CSF dynamics. Am J Neuroradiol 28: 983

    Google Scholar 

  • Kosteljanetz M (1989) Measurement of resistance to outflow: the bolus injection method. In: Gjerris F, Borgesen SE, Sorensen PS (eds) Proceedings Outflow of cerebrospinal fluid, pp 134–143

  • Lakin WD, Stevens SA, Tranmer BI, Penar PL (2003) A whole-body mathematical model for intracranial pressure dynamics. J Math Biol 46(4): 347

    Article  MATH  MathSciNet  Google Scholar 

  • Linninger AA, Tsakiris C, Zhu DC, Xenos M, Roycewicz P, Danziger Z, Penn RD (2005) Pulsatile cerebrospinal fluid dynamics in the human brain. IEEE Trans Biomed Eng 52(4): 557

    Article  Google Scholar 

  • Linninger AA, Xenos M, Zhu DC, Somayaji MR, Kondapalli S, Penn RD (2007) Cerebrospinal fluid flow in the normal and hydrocephalic human brain. IEEE Trans Biomed Eng 54(2): 291

    Article  Google Scholar 

  • Loth F, Yardimci AM, Alperin N (2001) Hydrodynamic modeling of cerebrospinal fluid motion within the spinal cavity. J Biomech Eng 123(1): 71

    Article  Google Scholar 

  • Luo XY, Pedley TJ (1998) The effects of wall inertia on flow in a two-dimensional collapsible channel. J Fluid Mech 363: 253

    Article  MATH  Google Scholar 

  • Marmarou A (1973) A theoretical model and experimental evaluation of the cerebrospinal fluid system. Thesis, Drexel University, Philadelphia, PA

  • Marmarou A, Shulman K, Rosende RM (1978) A nonlinear analysis of the cerebrospinal fluid system and intracranial pressure dynamics. J Neurosurg 48: 332

    Article  Google Scholar 

  • Nield D, Bejan A (1999) Convection in porous media. Springer, New York

    MATH  Google Scholar 

  • Pedley TJ (1980) The fluid mechanics of large blood vessels. Cambridge University Press, Cambridge

    MATH  Google Scholar 

  • Pelc NJ, Bernstein MA, Shimakawa A, Glover GH (1991) Encoding strategies for three-direction phase-contrast MR imaging of flow. J Magn Reson Imaging 1(4): 405

    Article  Google Scholar 

  • Penn RD, Lee MC, Linninger AA, Miesel K, Lu SN, Stylos L (2005) Pressure Gradients in the Brain in an experimental model of hydrocephalus. J Neurosurg 102(6): 1069

    Article  Google Scholar 

  • Pellicer A, Gaya F, Madero R, Quero J, Cabanas F (2006) Noninvasive continuous monitoring of the effect of head position on brain hemodynamics in ventilated infants. Pediatrics 109(3): 434

    Article  Google Scholar 

  • Piechnik SK, Czosnyka M, Harris NG, Minhas PS, Pickard JD (2001) A Model of the Cerebral and Cerebrospinal Fluid Circulations to Examine Asymmetry in Cerebrovascular Reactivity. J Cereb Blood Flow Metab 21: 182

    Article  Google Scholar 

  • Raksin PB, Alperin N, Sivaramakrishnan A, Surapaneni S, Lichtor T (2003) Noninvasive intracranial compliance and pressure based on dynamic magnetic resonance imaging of blood flow and cerebrospinal fluid flow: review of principles, implementation, and other noninvasive approaches. Neurosurg Focus 14(4): 1

    Article  Google Scholar 

  • Segal M (2001) Transport of nutrients across the choroid plexus. Microsc Res Tech 52: 38

    Article  Google Scholar 

  • Smillie A, Sobey I, Molnar Z (2005) A hydroelastic model of hydrocephalus. J Fluid Mech 539: 417

    Article  MATH  MathSciNet  Google Scholar 

  • Sorek S, Bear J, Karni Z (1988a) A non-steady compartmental flow model of the cerebrovascular system. J Biomech 21(9): 695

    Article  Google Scholar 

  • Sorek S, Feinsod M, Bear J (1988b) Can NPH be caused by cerebral small vessel disease? A new look based on a mathematical model. Med Biol Eng Comput 26(3): 310

    Article  Google Scholar 

  • Sorek S, Bear J, Karni Z (1989) Resistances and compliances of a compartmental model of the cerebrovascular system. Ann Biomed Eng 17(1): 1

    Article  Google Scholar 

  • Starling EH (1896) On the absorption of fluids from the connective tissue spaces. J Physiol 19: 312

    Google Scholar 

  • Stevens S (2000) Mean pressures and flows in the human intracranial system, determined by mathematical simulations of a steady-state infusion test. Neurol Res 22(8): 809

    Google Scholar 

  • Sweetman B (2007) Quantification of intracranial dynamics under normal and hydrocephalic conditions. Thesis, University of Illinois at Chicago, Chicago, IL

  • Ursino M, Lodi CA (1997) A simple mathematical model of the interaction between intracranial pressure and cerebral hemodynamics. J Appl Physiol 82(4): 1256

    Google Scholar 

  • Wilcox RK, Bilston LE, Barton DC, Hall RM (2003) Mathematical model for the viscoelastic properties of dura mater. J Orthop Sci 8: 432

    Article  Google Scholar 

  • Zagzoule M, Marc-Vergnes J (1986) A global mathematical model of the cerebral circulation in man. J Biomech 19(12): 1015

    Article  Google Scholar 

  • Zhang L, Kulkarni K, Somayaji MR, Xenos M, Linninger AA (2007) Discovery of transport and reaction properties in distributed systems. AIChE J 53(2): 381

    Article  Google Scholar 

  • Zhu DC, Xenos M, Linninger AA, Penn RD (2006) Dynamics of lateral ventricle and cerebrospinal fluid in normal and hydrocephalic brains. J Magn Reson Imaging 24(4): 756

    Article  Google Scholar 

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Correspondence to Andreas A. Linninger.

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Linninger, A.A., Xenos, M., Sweetman, B. et al. A mathematical model of blood, cerebrospinal fluid and brain dynamics. J. Math. Biol. 59, 729–759 (2009). https://doi.org/10.1007/s00285-009-0250-2

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  • DOI: https://doi.org/10.1007/s00285-009-0250-2

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