Cerebrospinal Fluid Hydrodynamics in Chiari I Malformation and Syringomyelia: Modeling Pathophysiology

John D Heiss, John D Heiss

Abstract

Anatomic MRI, MRI flow studies, and intraoperative ultrasonography demonstrate that the Chiari I malformation obstructs CSF pathways at the foramen magnum and prevents normal CSF movement through the foramen magnum. Impaired CSF displacement across the foramen magnum during the cardiac cycle increases pulsatile hindbrain motion, pressure transmission to the spinal subarachnoid space, and the amplitude of CSF subarachnoid pressure waves driving CSF into the spinal cord. Central canal septations in adults prevent syrinx formation by CSF directly transmitting its pressure wave from the fourth ventricle to the central canal.

Keywords: Aquaporin 4; Cerebrospinal fluid dynamics; Chiari I malformation; Foramen magnum decompression; Glymphatic system; Hydrocephalus; Pathophysiology; Syringomyelia.

Conflict of interest statement

Disclosure The author has nothing to disclose.

Published by Elsevier Inc.

Figures

Figure 1:
Figure 1:
The rigid skull surrounds the intracranial cavity (left), which is much less compliant than the spinal intradural space (right). The spinal dura (right) can expand into the epidural space during cardiac systole because of the surrounding compressible fat and veins and the ligamentum flavum covering the interlaminar spaces. CSF is normally driven across from the incompliant intracranial cavity to the more compliant spinal subarachnoid space to compensate for the volumetric expansion of intracranial arteries during cardiac systole.
Figure 2:
Figure 2:
During cardiac systole, the Chiari I malformation obstructs typical CSF displacement from the intracranial cavity to the spinal subarachnoid space. In place of CSF, the cerebellar tonsils and medulla are displaced inferiorly, creating an enlarged cervical subarachnoid pressure wave (A). The pressure wave propels syrinx fluid motion that elongates the syrinx (A). The pressure wave also drives CSF into the perivascular spaces of the spinal cord. It may oppose spinal cord interstitial fluid egress through the glymphatic system and into the spinal subarachnoid space (B). The distending force within the syrinx that expands the syrinx radially may arise from increased resistance to fluid outflow from the spinal cord central canal, syrinx, and spinal cord interstitial spaces to the spinal subarachnoid space (C).
Figure 3:
Figure 3:
Syrinx enlargement is a slow process that proceeds from the central canal and surrounding gray matter of the spinal cord. The growing syrinx initially stretches gray matter structures and the spinothalamic crossing tracts. Syrinx pressure can injure the central spinal cord structures irreversibly.
Figure 4:
Figure 4:
Syringes arise from diverse mechanisms that share the feature that they create a net increase in the intramedullary fluid.

References

    1. Chiari H. Concerning alterations in the cerebellum resulting from cerebral hydrocephalus. 1891. Pediatr Neurosci. 1987;13(1):3–8. doi:10.1159/000120293
    1. Mortazavi MM, Tubbs RS, Brockerhoff MA, Loukas M, Oakes WJ. The first description of Chiari I malformation with intuitive correlation between tonsillar ectopia and syringomyelia. J Neurosurg Pediatr. Mar 2011;7(3):257–60. doi:10.3171/2010.12.Peds10579
    1. Gardner WJ, Angel J. The mechanism of syringomyelia and its surgical correction. Clin Neurosurg. 1958;6:131–40. doi:10.1093/neurosurgery/6.cn_suppl_1.131
    1. Williams B The distending force in the production of “communicating syringomyelia”. Lancet. Jul 26 1969;2(7613):189–93. doi:10.1016/s0140-6736(69)91427-5
    1. Milhorat TH, Kotzen RM, Anzil AP. Stenosis of central canal of spinal cord in man: incidence and pathological findings in 232 autopsy cases. J Neurosurg. Apr 1994;80(4):716–22.
    1. Williams B. Syringomyelia. Neurosurg Clin N Am. Jul 1990;1(3):653–85.
    1. Haller G, Sadler B, Kuensting T, et al. Obex position is associated with syringomyelia and use of posterior fossa decompression among patients with Chiari I malformation. J Neurosurg Pediatr. Apr 10 2020;26(1):45–52. doi:10.3171/2020.2.PEDS19486
    1. Hirano M, Haughton V, Munoz del Rio A. Tapering of the cervical spinal canal in patients with Chiari I malformations. AJNR Am J Neuroradiol. Aug 2012;33(7):1326–30. doi:10.3174/ajnr.A2948
    1. Nishikawa M, Sakamoto H, Hakuba A, Nakanishi N, Inoue Y. Pathogenesis of Chiari malformation: a morphometric study of the posterior cranial fossa. J Neurosurg. Jan 1997;86(1):40–7. doi:10.3171/jns.1997.86.1.0040
    1. Noudel R, Jovenin N, Eap C, Scherpereel B, Pierot L, Rousseaux P. Incidence of basioccipital hypoplasia in Chiari malformation type I: comparative morphometric study of the posterior cranial fossa. Clinical article. J Neurosurg. Nov 2009;111(5):1046–52. doi:10.3171/2009.2.JNS08284
    1. Dlouhy BJ, Dawson JD, Menezes AH. Intradural pathology and pathophysiology associated with Chiari I malformation in children and adults with and without syringomyelia. J Neurosurg Pediatr. Dec 2017;20(6):526–541. doi:10.3171/2017.7.PEDS17224
    1. Guan J, Yuan C, Zhang C, et al. Intradural Pathology Causing Cerebrospinal Fluid Obstruction in Syringomyelia and Effectiveness of Foramen Magnum and Foramen of Magendie Dredging Treatment. World Neurosurg. Dec 2020;144:e178–e188. doi:10.1016/j.wneu.2020.08.068
    1. Orakdogen M, Emon ST, Erdogan B, Somay H. Fourth Ventriculostomy in Occlusion of the Foramen of Magendie Associated with Chiari Malformation and Syringomyelia. NMC Case Rep J. Apr 2015;2(2):72–75. doi:10.2176/nmccrj.2014-0245
    1. Milhorat TH. Classification of syringomyelia. Neurosurg Focus. Mar 15 2000;8(3):E1. doi:10.3171/foc.2000.8.3.1
    1. Longatti P, Fiorindi A, Marton E, Sala F, Feletti A. Where the central canal begins: endoscopic in vivo description. J Neurosurg. Mar 1 2022;136(3):895–904. doi:10.3171/2020.12.Jns203649
    1. . Hydrodynamics. merriam-webstercom: ; 2022.
    1. Heiss JD, Patronas N, DeVroom HL, et al. Elucidating the pathophysiology of syringomyelia. J Neurosurg. Oct 1999;91(4):553–62. doi:10.3171/jns.1999.91.4.0553
    1. Heiss JD, Suffredini G, Smith R, et al. Pathophysiology of persistent syringomyelia after decompressive craniocervical surgery. Clinical article. J Neurosurg Spine. Dec 2010;13(6):729–42. doi:10.3171/2010.6.SPINE10200
    1. Oldfield EH, Muraszko K, Shawker TH, Patronas NJ. Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. Implications for diagnosis and treatment. J Neurosurg. Jan 1994;80(1):3–15.
    1. Srivastava A, Sood A, Joy SP, Woodcock J. Principles of physics in surgery: the laws of flow dynamics physics for surgeons - Part 1. Indian J Surg. Aug 2009;71(4):182–7. doi:10.1007/s12262-009-0064-x
    1. Loth F, Yardimci MA, Alperin N. Hydrodynamic modeling of cerebrospinal fluid motion within the spinal cavity. J Biomech Eng. Feb 2001;123(1):71–9. doi:10.1115/1.1336144
    1. Pahlavian SH, Loth F, Luciano M, Oshinski J, Martin BA. Neural Tissue Motion Impacts Cerebrospinal Fluid Dynamics at the Cervical Medullary Junction: A Patient-Specific Moving-Boundary Computational Model. Ann Biomed Eng. Dec 2015;43(12):2911–23. doi:10.1007/s10439-015-1355-y
    1. Williams B, Sgouros S, Nenji E. Cerebrospinal fluid drainage for syringomyelia. Eur J Pediatr Surg. Dec 1995;5 Suppl 1:27–30.
    1. Muthukumar N Syringomyelia as a presenting feature of shunt dysfunction: Implications for the pathogenesis of syringomyelia. J Craniovertebr Junction Spine. Jan 2012;3(1):26–31. doi:10.4103/0974-8237.110125
    1. Del Bigio MR. The ependyma: a protective barrier between brain and cerebrospinal fluid. Glia. May 1995;14(1):1–13. doi:10.1002/glia.440140102
    1. Bruni JE. Ependymal development, proliferation, and functions: a review. Microsc Res Tech. Apr 1 1998;41(1):2–13. doi:10.1002/(sici)1097-0029(19980401)41:1<2::Aid-jemt2>;2-z
    1. Holly LT, Batzdorf U. Slitlike syrinx cavities: a persistent central canal. J Neurosurg. Sep 2002;97(2 Suppl):161–5. doi:10.3171/spi.2002.97.2.0161
    1. Thyagaraj S, Pahlavian SH, Sass LR, et al. An MRI-Compatible Hydrodynamic Simulator of Cerebrospinal Fluid Motion in the Cervical Spine. IEEE Trans Biomed Eng. Jul 2018;65(7):1516–1523. doi:10.1109/tbme.2017.2756995
    1. Leung V, Magnussen JS, Stoodley MA, Bilston LE. Cerebellar and hindbrain motion in Chiari malformation with and without syringomyelia. J Neurosurg Spine. Apr 2016;24(4):546–55. doi:10.3171/2015.8.Spine15325
    1. Ellertsson AB. Syringomyelia and other cystic spinal cord lesions. Acta Neurol Scand. 1969;45(4):403–17.
    1. Wei F, Zhang C, Xue R, et al. The pathway of subarachnoid CSF moving into the spinal parenchyma and the role of astrocytic aquaporin-4 in this process. Life Sci. Aug 1 2017;182:29–40. doi:10.1016/j.lfs.2017.05.028
    1. Oklinski MK, Lim JS, Choi FIJ, Oklinska P, Skowronski MT, Kwon TH. Immunolocalization of Water Channel Proteins AQP1 and AQP4 in Rat Spinal Cord. J Histochem Cytochem. Aug 2014;62(8):598–611. doi:10.1369/0022155414537495
    1. Hemley SJ, Bilston LE, Cheng S, Chan JN, Stoodley MA. Aquaporin-4 expression in post-traumatic syringomyelia. J Neurotrauma. Aug 15 2013;30(16):1457–67. doi:10.1089/neu.2012.2614
    1. Xiong A, Li J, Xiong R, et al. Inhibition of HIF-1α-AQP4 axis ameliorates brain edema and neurological functional deficits in a rat controlled cortical injury (CCI) model. Scl Rep. Feb 17 2022;12(1):2701. doi:10.1038/s41598-022-06773-9
    1. Vindedal GF, Thoren AE, Jensen V, et al. Removal of aquaporin-4 from glial and ependymal membranes causes brain water accumulation. Mol Cell Neurosci. Dec 2016;77:47–52. doi:10.1016/j.mcn.2016.10.004
    1. Storer KP, Toh J, Stoodley MA, Jones NR. The central canal of the human spinal cord: a computerised 3-D study. J Anat. May 1998;192 (Pt 4)(Pt 4):565–72. doi:10.1046/j.1469-7580.1998.19240565.x
    1. Koh L, Zakharov A, Johnston M. Integration of the subarachnoid space and lymphatics: is it time to embrace a new concept of cerebrospinal fluid absorption? Cerebrospinal Fluid Res. Sep 20 2005;2:6. doi:10.1186/1743-8454-2-6
    1. Levy EI, Heiss JD, Kent MS, Riedel CJ, Oldfield EH. Spinal cord swelling preceding syrinx development Case report. J Neurosurg. Jan 2000;92(1 Suppl):93–7. doi:10.3171/spi.2000.92.1.0093
    1. Takamura Y, Kawasaki T, Takahashi A, et al. A craniocervical injury-induced syringomyelia caused by central canal dilation secondary to acquired tonsillar herniation. Case report. J Neurosurg. Jul 2001;95(1 Suppl):122–7. doi:10.3171/spi.2001.95.1.0122
    1. Kedarasetti RT, Drew PJ, Costanzo F. Arterial vasodilation drives convective fluid flow in the brain: a poroelastic model. Fluids Barriers CNS. May 15 2022;19(1):34. doi:10.1186/s12987-022-00326-y
    1. Rasmussen MK, Mestre H, Nedergaard M. Fluid transport in the brain. Physiol Rev. Apr 1 2022; 102(2): 1025–1151. doi:10.1152/physrev.00031.2020
    1. Hammock MK, Milhorat TH. The cerebrospinal fluid: current concepts of its formation. Ann Clin Lab Sci. Jan-Feb 1976;6(1):22–6.
    1. Li Q, Aalling NN, Förstera B, et al. Aquaporin 1 and the Na(+)/K(+)/2Cl(−) cotransporter 1 are present in the leptomeningeal vasculature of the adult rodent central nervous system. Fluids Barriers CNS. Feb 11 2020;17(1):15. doi:10.1186/s12987-020-0176-z
    1. Milhorat TH, Hammock MK, Fenstermacher JD, Levin VA. Cerebrospinal fluid production by the choroid plexus and brain. Science. Jul 23 1971;173(3994):330–2. doi:10.1126/science.173.3994.330
    1. Trillo-Contreras JL, Toledo-Aral JJ, Echevarría M, Villadiego J. AQP1 and AQP4 Contribution to Cerebrospinal Fluid Homeostasis. Cells. Feb 24 2019;8(2)doi:10.3390/cells8020197
    1. Wetjen NM, Heiss JD, Oldfield EH. Time course of syringomyelia resolution following decompression of Chiari malformation Type I. J Neurosurg Pediatr. Feb 2008;1(2):118–23. doi:10.3171/PED/2008/l/2/118
    1. Vaquero J, Ferreira E, Parajón A. Spontaneous resolution of syrinx: report of two cases in adults with Chiari malformation. Neurol Sci. Apr 2012;33(2):339–41. doi:10.1007/s10072-011-0670-9
    1. Rhoton ALJ. Microsurgery of syringomyelia and syringomyelic cord syndrome. In: Schmidek HH, Sweet WH, eds. Operative Neurosurgical Techniques. WB Saunders; 1988:1307–1326.
    1. Milhorat TH, Capocelli AL Jr, Kotzen RM, Bolognese P, Heger IM, Cottrell JE. Intramedullary pressure in syringomyelia: clinical and pathophysiological correlates of syrinx distension. Neurosurgery. Nov 1997;41(5):1102–10.
    1. Heiss JD, Jarvis K, Smith RK, et al. Origin of Syrinx Fluid in Syringomyelia: A Physiological Study. Neurosurgery. Feb 1 2019;84(2):457–468. doi:10.1093/neuros/nyy072
    1. Melhem ER, Jara H, Eustace S. Fluid-attenuated inversion recovery MR imaging: identification of protein concentration thresholds for CSF hyperintensity. AJR Am J Roentgenol. Sep 1997;169(3):859–62. doi:10.2214/ajr.169.3.9275912
    1. Shtaya A, Sadek AR, Nicoll JAR, Nader-Sepahi A. Choroid Plexus in the Central Canal of the Spinal Cord Causing Recurrent Syringomyelia. World Neurosurg. Mar 2018;111:275–278. doi:10.1016/j.wneu.2017.12.143
    1. Moore SA. The Spinal Ependymal Layer in Health and Disease. Vet Pathol. Jul 2016;53(4):746–53. doi:10.1177/0300985815618438
    1. . Hydrostatics. merriam-webstercom: ; 2022.
    1. Schlesinger EB, Antunes JL, Michelsen WJ, Louis KM. Hydromyelia: clinical presentation and comparison of modalities of treatment. Neurosurgery. Oct 1981;9(4):356–65.
    1. Ramo NL, Troyer KL, Puttlitz CM. Viscoelasticity of spinal cord and meningeal tissues. Acta Biomater. Jul 15 2018;75:253–262. doi:10.1016/j.actbio.2018.05.045
    1. Bilston LE, Thibault LE. The mechanical properties of the human cervical spinal cord in vitro. Ann Biomed Eng. Jan-Feb 1996;24(1):67–74. doi:10.1007/bf02770996
    1. Itoh T, Nishimura R, Matsunaga S, Kadosawa T, Mochizuki M, Sasaki N. Syringomyelia and hydrocephalus in a dog. J Am Vet Med Assoc. Sep 1 1996;209(5):934–6.
    1. Plessas IN, Rusbridge C, Driver CJ, et al. Long-term outcome of Cavalier King Charles spaniel dogs with clinical signs associated with Chiari-like malformation and syringomyelia. Vet Rec. Nov 17 2012;171(20):501. doi:10.1136/vr.100449

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться