Spinal subarachnoid space pressure measurements in an in vitro spinal stenosis model: Implications on syringomyelia theories

Journal of Biomechanical Engineering

Volumn 132, Issue 11, 2010, Pages

  Martin, Bryn A ^a   Labuda, Richard ^b   Royston, Thomas J ^c   Oshinski, John N ^d   Iskandar, Bermans ^e   Loth, Francis ^f  

^a EPFL   (Switzerland)

^b Chiari and Syringomyelia Patient Education Foundation   (United States)

^c University of Illinois at Chicago   (United States)

^d EMORY UNIVERSITY   (United States)

^e UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^f UNIVERSITY OF AKRON   (United States)

Author keywords

Cerebrospinal fluid hydrodynamics; Chiari malformation; Fluid structure interaction; Hydrocephalus; In vitro model; Intracranial and spinal pressures; Spinal cord; Subarachnoid space stenosis; Syringomyelia; Syrinx

Indexed keywords

CEREBROSPINAL FLUID HYDRODYNAMICS; CHIARI MALFORMATION; HYDROCEPHALUS; IN VITRO MODEL; INTRACRANIAL AND SPINAL PRESSURES; SPINAL CORD; SUBARACHNOID SPACE STENOSIS; SYRINGOMYELIA;

BODY FLUIDS; BRAIN; DOSIMETRY; FLUID DYNAMICS; FLUID STRUCTURE INTERACTION; FLUIDS; HYDRODYNAMICS; PRESSURE MEASUREMENT;

ELECTRIC FAULT CURRENTS;

ARNOLD CHIARI MALFORMATION; ARTICLE; CEREBROSPINAL FLUID FLOW; CEREBROSPINAL FLUID PRESSURE; ELASTICITY; GEOMETRY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PAIN; PRESSURE MEASUREMENT; SPINE; SUBARACHNOID SPACE; SYRINGOMYELIA; THEORY; VERTEBRAL CANAL STENOSIS; BIOLOGICAL MODEL; BIOMECHANICS; CEREBROSPINAL FLUID; COMPLIANCE (PHYSICAL); PATHOPHYSIOLOGY; PERMEABILITY; PHYSIOLOGY;

ARNOLD-CHIARI MALFORMATION; BIOMECHANICS; CEREBROSPINAL FLUID PRESSURE; COMPLIANCE; ELASTICITY; HUMANS; MODELS, NEUROLOGICAL; PERMEABILITY; SPINAL STENOSIS; SUBARACHNOID SPACE; SYRINGOMYELIA;

EID: 77958588951     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.4000089     Document Type: Article

References (70)

1. Heiss J.D. Patronas N. DeVroom H.L. Shawker T. Ennis R. Kammerer W. Eidsath A. Talbot T. Morris J. Eskioglu E. Oldfield E.H. Elucidating the Pathophysiology of Syringomyelia. J. Neurosurg. 1999, 91(4):553-562. JONSAC, 0022-3085, 10.3171/jns.1999.91.4.0553.
2. Williams B. Cerebrospinal Fluid Pressure Changes in Response to Coughing. Brain 1976, 99(2):331-346. BRAIAK, 0006-8950, 10.1093/brain/99.2.331.
3. Williams B. Simultaneous Cerebral and Spinal Fluid Pressure Recordings. 2. Cerebrospinal Dissociation With Lesions at the Foramen Magnum. Acta Neurochir. 1981, 59(1-2):123-142. ACNUA5, 0001-6268, 10.1007/BF01411198.
4. Williams B. Simultaneous Cerebral and Spinal Fluid Pressure Recordings. I. Technique, Physiology, and Normal Results. Acta Neurochir. 1981, 58(3-4):167-185. ACNUA5, 0001-6268, 10.1007/BF01407124.
5. Williams B. On the Pathogenesis of Syringomyelia: A Review. J. R. Soc. Med. 1980, 73(11):798-806. JRSMD9, 0141-0768.
6. Milhorat T.H. Capocelli Jr. A.L. Kotzen R.M. Bolognese P. Heger I.M. Cottrell J.E. Intramedullary Pressure in Syringomyelia: Clinical and Pathophysiological Correlates of Syrinx Distension. Neurosurgery 1997, 41(5):1102-1110. 0148-396X, 10.1097/00006123-199711000-00014.
7. Williams B. Experimental Communicating Syringomyelia in Dogs After Cisternal Kaolin Injection. Part 2. Pressure Studies. J. Neurol. Sci. 1980, 48(1):109-122. JNSCAG, 0022-510X, 10.1016/0022-510X(80)90154-9.
8. Williams B. Bentley J. Experimental Communicating Syringomyelia in Dogs After Cisternal Kaolin Injection. Part 1. Morphology. J. Neurol. Sci. 1980, 48(1):93-107. JNSCAG, 0022-510X, 10.1016/0022-510X(80)90153-7.
9. Hall P. Turner M. Aichinger S. Bendick P. Campbell R. Experimental Syringomyelia: The Relationship Between Intraventricular and Intrasyrinx Pressures. J. Neurosurg. 1980, 52(6):812-817. JONSAC, 0022-3085, 10.3171/jns.1980.52.6.0812.
10. Stoodley M.A. Brown S.A. Brown C.J. Jones N.R. Arterial Pulsation-Dependent Perivascular Cerebrospinal Fluid Flow Into the Central Canal in the Sheep Spinal Cord. J. Neurosurg. 1997, 86(4):686-693. JONSAC, 0022-3085, 10.3171/jns.1997.86.4.0686.
11. Klekamp J. Volkel K. Bartels C.J. Samii M. Disturbances of Cerebrospinal Fluid Flow Attributable to Arachnoid Scarring Cause Interstitial Edema of the Cat Spinal Cord. Neurosurgery 2001, 48(1):174-185. 0148-396X, 10.1097/00006123-200101000-00031.
12. Martin B.A. Kalata W. Loth F. Royston T.J. Oshinski J.N. Syringomyelia Hydrodynamics: An In Vitro Study Based on In Vivo Measurements. J. Biomech. Eng. 2005, 127(7):1110-1120. JBENDY, 0148-0731, 10.1115/1.2073687.
13. Carpenter P.W. Berkouk K. Lucey A.D. Pressure Wave Propagation in Fluid-Filled Co-Axial Elastic Tubes. Part 2: Mechanisms for the Pathogenesis of Syringomyelia. ASME J. Biomech. Eng. 2003, 125(6):857-863. JBENDY, 0148-0731, 10.1115/1.1634281.
14. Berkouk K. Carpenter P.W. Lucey A.D. Pressure Wave Propagation in Fluid-Filled Co-Axial Elastic Tubes. Part 1: Basic Theory. ASME J. Biomech. Eng. 2003, 125(6):852-856. JBENDY, 0148-0731, 10.1115/1.1634280.
15. Bertram C.D. Bilston L.E. Stoodley M.A. Tensile Radial Stress in the Spinal Cord Related to Arachnoiditis or Tethering: A Numerical Model. Med. Biol. Eng. Comput. 2008, 46(7):701-707. MBECDY, 0140-0118, 10.1007/s11517-008-0332-0.
16. Bertram C.D. Brodbelt A.R. Stoodley M.A. The Origins of Syringomyelia: Numerical Models of Fluid/Structure Interactions in the Spinal Cord. ASME J. Biomech. Eng. 2005, 127(7):1099-1109. JBENDY, 0148-0731, 10.1115/1.2073607.
17. Bilston L.E. Fletcher D.F. Brodbelt A.R. Stoodley M.A. Arterial Pulsation-Driven Cerebrospinal Fluid Flow in the Perivascular Space: A Computational Model. Comput. Methods Biomech. Biomed. Eng. 2003, 6(4):235-241. CMBEFS, 1025-5842, 10.1080/10255840310001606116.
18. Loth F. Yardimci M.A. Alperin N. Hydrodynamic Modeling of Cerebrospinal Fluid Motion Within the Spinal Cavity. ASME J. Biomech. Eng. 2001, 123(1):71-79. JBENDY, 0148-0731, 10.1115/1.1336144.
19. Chang H.S. Nakagawa H. Hypothesis on the Pathophysiology of Syringomyelia Based on Simulation of Cerebrospinal Fluid Dynamics. J. Neurol., Neurosurg. Psychiatry 2003, 74(3):344-347. JNNPAU, 0022-3050, 10.1136/jnnp.74.3.344.
20. Alperin N.J. Lee S.H. Loth F. Raksin P.B. Lichtor T. MR-Intracranial Pressure (ICP): A Method to Measure Intracranial Elastance and Pressure Noninvasively by Means of MR Imaging: Baboon and Human Study. Radiology 2000, 217(3):877-885. RADLAX, 0033-8419.
21. Gardner W.J. Angel J. The Mechanism of Syringomyelia and Its Surgical Correction. Clin. Neurosurg. 1958, 6:131-140. CLNEA8, 0069-4827.
22. Gardner W.J. Hydrodynamic Mechanism of Syringomyelia: Its Relationship to Myelocele. J. Neurol. Neurosurg. Psychiatry 1965, 28:247-259. 10.1136/jnnp.28.3.247.
23. Williams B. The Distending Force in the Production of Communicating Syringomyelia. Lancet 1969, 294(7622):696-697. LANCAO, 0140-6736, 10.1016/S0140-6736(69)90406-1.
24. Williams B. A Critical Appraisal of Posterior Fossa Surgery for Communicating Syringomyelia. Brain 1978, 101(2):223-250. BRAIAK, 0006-8950, 10.1093/brain/101.2.223.
25. Itabashi T. Quantitative Analysis of Cervical CSF and Syrinx Fluid Pulsations. Nippon Seikeigeka Gakkai Zasshi 1990, 64(7):523-533. 0021-5325.
26. Enzmann D.R. O'Donohue J. Rubin J.B. Shuer L. Cogen P. Silverberg G. CSF Pulsations Within Nonneoplastic Spinal Cord Cysts. AJR, Am. J. Roentgenol. 1987, 149(1):149-157. AAJRDX, 0361-803X.
27. Ball M.J. Dayan A.D. Pathogenesis of Syringomyelia. Lancet 1972, 300(7781):799-801. LANCAO, 0140-6736, 10.1016/S0140-6736(72)92152-6.
28. Weller R.O. Pathology of Cerebrospinal Fluid and Interstitial Fluid of the CNS: Significance for Alzheimer Disease, Prion Disorders and Multiple Sclerosis. J. Neuropathol. Exp. Neurol. 1998, 57(10):885-894. JNENAD, 0022-3069, 10.1097/00005072-199810000-00001.
29. Zhang E.T. Inman C.B. Weller R.O. Interrelationships of the Pia Mater and the Perivascular (Virchow-Robin) Spaces in the Human Cerebrum. J. Anat. 1990, 170:111-123. JOANAY, 0021-8782.
30. Stoodley M.A. Jones N.R. Brown C.J. Evidence for Rapid Fluid Flow From the Subarachnoid Space Into the Spinal Cord Central Canal in the Rat. Brain Res. 1996, 707(2):155-164. BRREAP, 0006-8993, 10.1016/0006-8993(95)01228-1.
31. Oldfield E.H. Muraszko K. Shawker T.H. Patronas N.J. Pathophysiology of Syringomyelia Associated With Chiari I Malformation of the Cerebellar Tonsils. Implications for Diagnosis and Treatment. J. Neurosurg. 1994, 80(1):3-15. JONSAC, 0022-3085, 10.3171/jns.1994.80.1.0003.
32. Greitz D. Unraveling the Riddle of Syringomyelia. Neurosurg. Rev. 2006, 29(4):251-264. 0344-5607, 10.1007/s10143-006-0029-5.
33. Brodbelt A.R. Stoodley M.A. Watling A.M. Tu J. Jones N.R. Fluid Flow in an Animal Model of Post-Traumatic Syringomyelia. Eur. Spine J. 2003, 12(3):300-306. 0940-6719, 10.1007/s00586-002-0492-9.
34. Stoodley M.A. Pathophysiology of Syringomyelia. J. Neurosurg. 2000, 92(6):1069-1070. JONSAC, 0022-3085.
35. Brodbelt A.R. Brown C.J. Jones N.R. Time and Dose Profiles of Experimental Excitotoxic Post-Traumatic Syringomyelia (Abstract). Aust. N. Z. J. Surg. 2001, 71(A66). 0004-8682.
36. Brodbelt A.R. Stoodley M.A. Watling A.M. Tu J. Burke S. Jones N.R. Altered Subarachnoid Space Compliance and Fluid Flow in an Animal Model of Posttraumatic Syringomyelia. Spine 2003, 28(20):E413-E419. SPINDD, 0362-2436, 10.1097/01.BRS.0000092346.83686.B9.
37. Stoodley M.A. Gutschmidt B. Jones N.R. Cerebrospinal Fluid Flow in an Animal Model of Noncommunicating Syringomyelia. Neurosurgery 1999, 44(5):1065-1075. 0148-396X, 10.1097/00006123-199905000-00068.
38. Stoodley M.A. Jones N.R. Yang L. Brown C.J. Mechanisms Underlying the Formation and Enlargement of Noncommunicating Syringomyelia: Experimental Studies. Neurosurg. Focus 2000, 8(3):1-7. 10.3171/foc.2000.8.3.2.
39. Storer K.P. Toh J. Stoodley M.A. Jones N.R. The Central Canal of the Human Spinal Cord: A Computerised 3-D Study. J. Anat. 1998, 192(4):565-572. JOANAY, 0021-8782, 10.1046/j.1469-7580.1998.19240565.x.
40. Brodbelt A.R. Stoodley M.A. Post-Traumatic Syringomyelia: A Review. J. Clin. Neurosci. 2003, 10(4):401-408. 10.1016/S0967-5868(02)00326-0.
41. Wagner Jr. F.C. Stewart W.B. Effect of Trauma Dose on Spinal Cord Edema. J. Neurosurg. 1981, 54(6):802-806. JONSAC, 0022-3085, 10.3171/jns.1981.54.6.0802.
42. Davis C.H. Symon L. Mechanisms and Treatment in Post-Traumatic Syringomyelia. Br. J. Neurosurg. 1989, 3(6):669-674. 0268-8697, 10.3109/02688698908992690.
43. Bilston L.E. Stoodley M.A. Fletcher D.F. The Influence of the Relative Timing of Arterial and Subarachnoid Space Pulse Waves on Spinal Perivascular Cerebrospinal Fluid Flow as a Possible Factor in Syrinx Development. J. Neurosurg. 2009, 112:808-813. JONSAC, 0022-3085.
44. Levine D.N. The Pathogenesis of Syringomyelia Associated With Lesions at the Foramen Magnum: A Critical Review of Existing Theories and Proposal of a New Hypothesis. J. Neurol. Sci. 2004, 220(1-2):3-21. JNSCAG, 0022-510X, 10.1016/j.jns.2004.01.014.
45. Klekamp J. The Pathophysiology of Syringomyelia-Historical Overview and Current Concept. Acta Neurochir. 2002, 144(7):649-664. ACNUA5, 0001-6268, 10.1007/s00701-002-0944-3.
46. Perrin R.G. Fehlings M. The Etiology of Syringomyelia in Association With Lesions of the Foramen Magnum. J. Neurol. Sci. 2004, 220(1-2):1-2. JNSCAG, 0022-510X, 10.1016/j.jns.2004.02.016.
47. Iskandar B.J. Hedlund G.L. Grabb P.A. Oakes W.J. The Resolution of Syringohydromyelia Without Hindbrain Herniation After Posterior Fossa Decompression. J. Neurosurg. 1998, 89(2):212-216. JONSAC, 0022-3085, 10.3171/jns.1998.89.2.0212.
48. Cirovic S. A Coaxial Tube Model of the Cerebrospinal Fluid Pulse Propagation in the Spinal Column. ASME J. Biomech. Eng. 2009, 131(2):021008. JBENDY, 0148-0731, 10.1115/1.3005159, p.
49. Cirovic S. Walsh C. Fraser W.D. Wave Propagation in a System of Coaxial Tubes Filled With Incompressible Media: A Model of Pulse Transmission in the Intracranial Arteries. J. Fluids Struct. 2002, 16(8):1029-1049. 0889-9746, 10.1006/jfls.2002.0457.
50. Elliott N.S. J. Lockerby D.A. Broadbelt A.R. The Pathogenesis of Syringomyelia: A Re-Evaluation of the Elastic Jump Hypothesis. ASME J. Biomech. Eng. 2009, 131:044503. JBENDY, 0148-0731, 10.1115/1.3072894.
51. Bilston L.E. Fletcher D.F. Stoodley M.A. Focal Spinal Arachnoiditis Increases Subarachnoid Space Pressure: A Computational Study. Clin. Biomech. (Bristol, Avon) 2006, 21(6):579-584. 0268-0033, 10.1016/j.clinbiomech.2006.01.009.
52. Pillay P.K. Awad I.A. Little J.R. Hahn J.F. Symptomatic Chiari Malformation in Adults: A New Classification Based on Magnetic Resonance Imaging With Clinical and Prognostic Significance. Neurosurgery 1991, 28(5):639-645. 0148-396X, 10.1097/00006123-199105000-00001.
53. Roosen N. Dahlhaus P. Lumenta C.B. Lins E. Stork W. Gahlen D. Bock W.J. Magnetic Resonance (MR) Imaging in the Management of Primary and Secondary Syringomyelic Cavities, and of Other Cystic Lesions of the Spinal Cord. Acta Neurochir. Suppl. (Wien) 1988, 93:13-16. 0065-1419, 10.1007/BF01409896.
54. Zarzur E. Mechanical Properties of the Human Lumbar Dura Mater. Arq. Neuropsiquiatr. 1996, 54(3):455-460. 0004-282X.
55. Patin D.J. Eckstein E.C. Harum K. Pallares V.S. Anatomic and Biomechanical Properties of Human Lumbar Dura Mater. Anesth. Analg. (Paris) 1993, 76(3):535-540. 0003-3014.
56. Ozawa H. Matsumoto T. Ohashi T. Sato M. Kokubun S. Mechanical Properties and Function of the Spinal Pia Mater. J. Neurosurg. Spine 2004, 1(1):122-127. 10.3171/spi.2004.1.1.0122.
57. Oakland R.J. Hall R.M. Wilcox R.K. Barton D.C. The Biomechanical Response of Spinal Cord Tissue to Uniaxial Loading. Proc. Inst. Mech. Eng., Part H: J. Eng. Med. 2006, 220(4):489-492. PIHMEQ, 0954-4119, 10.1243/09544119JEIM135.
58. Fiford R.J. Bilston L.E. The Mechanical Properties of Rat Spinal Cord In Vitro. J. Biomech. 2005, 38(7):1509-1515. JBMCB5, 0021-9290, 10.1016/j.jbiomech.2004.07.009.
59. Gefen A. Margulies S.S. Are In Vivo and In Situ Brain Tissues Mechanically Similar?. J. Biomech. 2004, 37(9):1339-1352. JBMCB5, 0021-9290, 10.1016/j.jbiomech.2003.12.032, and pp.
60. Bloomfield I.G. Johnston I.H. Bilston L.E. Effects of Proteins, Blood Cells and Glucose on the Viscosity of Cerebrospinal Fluid. Pediatr. Neurosurg. 1998, 28(5):246-251. 1016-2291, 10.1159/000028659.
61. Nakamura M. Chiba K. Nishizawa T. Maruiwa H. Matsumoto M. Toyama Y. Retrospective Study of Surgery-Related Outcomes in Patients With Syringomyelia Associated With Chiari I Malformation: Clinical Significance of Changes in the Size and Localization of Syrinx on Pain Relief. J. Neurosurg. Spine 2004, 100(3):241-244. 10.3171/spi.2004.100.3.0241.
62. Williams B. The Distending Force in the Production of Communicating Syringomyelia. Lancet 1970, 296(7662):41-42. LANCAO, 0140-6736, 10.1016/S0140-6736(70)92502-X.
63. Lichtor T. Egofske P. Alperin N. Noncommunicating Cysts and Cerebrospinal Fluid Flow Dynamics in a Patient With a Chiari I Malformation and Syringomyelia-Part II. Spine 2005, 30(12):1466-1472. SPINDD, 0362-2436, 10.1097/01.brs.0000164120.49208.1d.
64. Greitz D. Ericson K. Flodmark O. Pathogenesis and Mechanics of Spinal Cord Cyst. A New Hypothesis Based on Magnetic Resonance Studies of Cerbrospinal Fluid Dynamics. Int. J. Neuroradiology 1999, 5(2):61-78. and pp.
65. Levy E.I. Heiss J.D. Kent M.S. Riedel C.J. Oldfield E.H. Spinal Cord Swelling Preceding Syrinx Development. Case Report. J. Neurosurg. 2000, 92(1):93-97. JONSAC, 0022-3085.
66. Ravaglia S. Bogdanov E.I. Pichiecchio A. Bergamaschi R. Moglia A. Mikhaylov I.M. Pathogenetic Role of Myelitis for Syringomyelia. Clin. Neurol. Neurosurg. 2007, 109(6):541-546. 0303-8467, 10.1016/j.clineuro.2007.03.007.
67. Milhorat T.H. Capocelli Jr. A.L. Anzil A.P. Kotzen R.M. Milhorat R.H. Pathological Basis of Spinal Cord Cavitation in Syringomyelia: Analysis of 105 Autopsy Cases. J. Neurosurg. 1995, 82(5):802-812. JONSAC, 0022-3085, 10.3171/jns.1995.82.5.0802.
68. Milhorat T.H. Classification of Syringomyelia. Neurosurg. Focus 2000, 8(3):1-6. 10.3171/foc.2000.8.3.1.
69. Royo-Salvador M.B. Sole-Llenas J. Domenech J.M. Gonzalez-Adrio R. Results of the Section of the Filum Terminale in 20 Patients With Syringomyelia, Scoliosis and Chiari Malformation. Acta Neurochir. 2005, 147:515-523. ACNUA5, 0001-6268, 10.1007/s00701-005-0482-y.
70. Sansur C.A. Heiss J.D. DeVroom H.L. Eskioglu E. Ennis R. Oldfield E.H. Pathophysiology of Headache Associated With Cough in Patients With Chiari I Malformation. J. Neurosurg. 2003, 98(3):453-458. JONSAC, 0022-3085, 10.3171/jns.2003.98.3.0453.