Elucidating the pathophysiology of syringomyelia

Restricted access

Object. Syringomyelia causes progressive myelopathy. Most patients with syringomyelia have a Chiari I malformation of the cerebellar tonsils. Determination of the pathophysiological mechanisms underlying the progression of syringomyelia associated with the Chiari I malformation should improve strategies to halt progression of myelopathy.

Methods. The authors prospectively studied 20 adult patients with both Chiari I malformation and symptomatic syringomyelia. Testing before surgery included the following: clinical examination; evaluation of anatomy by using T1-weighted magnetic resonance (MR) imaging; evaluation of the syrinx and cerebrospinal fluid (CSF) velocity and flow by using phase-contrast cine MR imaging; and evaluation of lumbar and cervical subarachnoid pressure at rest, during the Valsalva maneuver, during jugular compression, and following removal of CSF (CSF compliance measurement). During surgery, cardiac-gated ultrasonography and pressure measurements were obtained from the intracranial, cervical subarachnoid, and lumbar intrathecal spaces and syrinx. Six months after surgery, clinical examinations, MR imaging studies, and CSF pressure recordings were repeated. Clinical examinations and MR imaging studies were repeated annually. For comparison, 18 healthy volunteers underwent T1-weighted MR imaging, cine MR imaging, and cervical and lumbar subarachnoid pressure testing.

Compared with healthy volunteers, before surgery, the patients had decreased anteroposterior diameters of the ventral and dorsal CSF spaces at the foramen magnum. In patients, CSF velocity at the foramen magnum was increased, but CSF flow was reduced. Transmission of intracranial pressure across the foramen magnum to the spinal subarachnoid space in response to jugular compression was partially obstructed. Spinal CSF compliance was reduced, whereas cervical subarachnoid pressure and pulse pressure were increased. Syrinx fluid flowed inferiorly during systole and superiorly during diastole on cine MR imaging. At surgery, the cerebellar tonsils abruptly descended during systole and ascended during diastole, and the upper pole of the syrinx contracted in a manner synchronous with tonsillar descent and with the peak systolic cervical subarachnoid pressure wave. Following surgery, the diameter of the CSF passages at the foramen magnum increased compared with preoperative values, and the maximum flow rate of CSF across the foramen magnum during systole increased. Transmission of pressure across the foramen magnum to the spinal subarachnoid space in response to jugular compression was normal and cervical subarachnoid mean pressure and pulse pressure decreased to normal. The maximum syrinx diameter decreased on MR imaging in all patients. Cine MR imaging documented reduced velocity and flow of the syrinx fluid. Clinical symptoms and signs improved or remained stable in all patients, and the tonsils resumed a normal shape.

Conclusions. The progression of syringomyelia associated with Chiari I malformation is produced by the action of the cerebellar tonsils, which partially occlude the subarachnoid space at the foramen magnum and act as a piston on the partially enclosed spinal subarachnoid space. This creates enlarged cervical subarachnoid pressure waves that compress the spinal cord from without, not from within, and propagate syrinx fluid caudally with each heartbeat, which leads to syrinx progression. The disappearance of the abnormal shape and position of the tonsils after simple decompressive extraarachnoidal surgery suggests that the Chiari I malformation of the cerebellar tonsils is acquired, not congenital. Surgery limited to suboccipital craniectomy, C-1 laminectomy, and duraplasty eliminates this mechanism and eliminates syringomyelia and its progression without the risk of more invasive procedures.

Article Information

Address reprint requests to: John D. Heiss, M.D., Surgical Neurology Branch, National Institutes of Health, 10 Center Drive, 10–5D37, MSC-1414, Bethesda, Maryland 20892–1414. email: heissjd@codon.nih.gov.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Graphs showing AP diameters of the subarachnoid space at the foramen magnum in healthy volunteers (normal subjects) and in patients with both Chiari I malformation and syringomyelia, before and after surgery. Diameters were measured ventral to the medulla (upper) and dorsal to the cerebellar tonsils (lower).

  • View in gallery

    Magnetic resonance T1-weighted images of the posterior fossa and cervical spine obtained in the midsagittal plane before surgery (left) and after craniocervical decompression and duraplasty (right). After decompressive surgery, the cerebellar tonsils become round and ascend into the posterior fossa, and the subarachnoid space is enlarged ventrally and dorsally. Horizontal black line is added to align the images at the foramen magnum.

  • View in gallery

    Pressure recordings showing partial occlusion of CSF flow at the foramen magnum. The rate of rise in intrathecal pressure is shown in a healthy volunteer (normal subject) and in a patient with both Chiari I malformation and syringomyelia before surgery and before the craniocervical junction is decompressed during surgery. After surgery, the rise in intrathecal pressure becomes normal. icp = intracranial pressure; lum = lumbar; s = seconds.

  • View in gallery

    Scatterplots in which the rates of rise in intrathecal pressure in patients with both Chiari I malformation and syringomyelia with those of healthy volunteers (normal subjects) are compared. After surgery, the rise in intrathecal pressure becomes normal.

  • View in gallery

    Graphs displaying the results of phase-contrast cine MR imaging studies obtained in patients and healthy volunteers (normal subjects). In each patient and volunteer, velocity was measured during 16 segments of the cardiac cycle. The mean velocity values for patients and healthy volunteers were plotted against the fraction of the cardiac cycle after the R-wave of the electrocardiogram. Positive values indicate caudal flow, and negative values indicate rostral flow. Error bars indicate 1 standard deviation from the mean. Upper: Velocity of CSF in the subarachnoid space at the foramen magnum. Lower: Velocity of syrinx fluid in patients before and after surgery.

  • View in gallery

    Scatterplot showing that craniospinal compliance was compromised before surgery and returned to normal after surgery. Compliance was measured by dividing the amount of CSF removed (10 ml) by the reduction in intrathecal pressure (in millimeters of mercury) that resulted.

  • View in gallery

    Graphs showing the measurement of syrinx diameter at C-2 by using cardiac-gated, intraoperative ultrasonography simultaneously with pressure recordings within the syrinx and cervical subarachnoid space. The syrinx contracts during cardiac systole when cervical subarachnoid pressure reaches its peak.

  • View in gallery

    Illustrations showing normal anatomy and flow of CSF in the subarachnoid space at the foramen magnum during the cardiac cycle in a normal healthy volunteer (upper); obstructed flow of CSF in the subarachnoid space at the foramen magnum resulting in the cerebellar tonsils' acting as a piston on the cervical subarachnoid space, creating cervical subarachnoid pressure waves that compress the spinal cord from without and propagating syrinx fluid movement (center); and relief of the obstruction of the subarachnoid space at the foramen magnum, eliminating the mechanism of progression of syringomyelia (lower).

References

  • 1.

    Barkovich AJWippold FJSherman JLet al: Significance of cerebellar tonsillar position on MR. AJNR 7:7957991986Barkovich AJ Wippold FJ Sherman JL et al: Significance of cerebellar tonsillar position on MR. AJNR 7:795–799 1986

    • Search Google Scholar
    • Export Citation
  • 2.

    Barnett HJMFoster JBHudgson P: Syringomyelia. Philadelphia: WB Saunders1973 pp 79103Barnett HJM Foster JB Hudgson P: Syringomyelia. Philadelphia: WB Saunders 1973 pp 79–103

    • Search Google Scholar
    • Export Citation
  • 3.

    Batzdorf U: Syringomyelia related to abnormalities at the level of the craniovertebral junction in Batzdorf U (ed): Syringomyelia: Current Concepts in Diagnosis and Treatment. Baltimore: Williams & Wilkins1991 pp 163182Batzdorf U: Syringomyelia related to abnormalities at the level of the craniovertebral junction in Batzdorf U (ed): Syringomyelia: Current Concepts in Diagnosis and Treatment. Baltimore: Williams & Wilkins 1991 pp 163–182

    • Search Google Scholar
    • Export Citation
  • 4.

    Boiardi AMunari LSilvani Aet al: Natural history and postsurgical outcome of syringomyelia. Ital J Neurol Sci 12:5755791991Boiardi A Munari L Silvani A et al: Natural history and postsurgical outcome of syringomyelia. Ital J Neurol Sci 12:575–579 1991

    • Search Google Scholar
    • Export Citation
  • 5.

    Boman KIivanainen M: Prognosis of syringomyelia. Acta Neurol Scand 43:61681967Boman K Iivanainen M: Prognosis of syringomyelia. Acta Neurol Scand 43:61–68 1967

    • Search Google Scholar
    • Export Citation
  • 6.

    Brewis MPoskanzer DCRolland Cet al: Neurological disease in an English city. Acta Neurologica Scand Suppl 24:1891966Brewis M Poskanzer DC Rolland C et al: Neurological disease in an English city. Acta Neurologica Scand Suppl 24:1–89 1966

    • Search Google Scholar
    • Export Citation
  • 7.

    Gardner WJAngel J: The mechanism of syringomyelia and its surgical correction. Clin Neurosurg 6:1311401959Gardner WJ Angel J: The mechanism of syringomyelia and its surgical correction. Clin Neurosurg 6:131–140 1959

    • Search Google Scholar
    • Export Citation
  • 8.

    Lakke JPWF: Queckenstedt's Test. Electromanometric Examination of CSF Pressure on Jugular Compression and its Clinical Value. Amsterdam: Excerpta Medica1969Lakke JPWF: Queckenstedt's Test. Electromanometric Examination of CSF Pressure on Jugular Compression and its Clinical Value. Amsterdam: Excerpta Medica 1969

    • Search Google Scholar
    • Export Citation
  • 9.

    Mariani CCislaghi MGBarbieri Set al: The natural history and results of surgery in 50 cases of syringomyelia. J Neurol 238:4334381991Mariani C Cislaghi MG Barbieri S et al: The natural history and results of surgery in 50 cases of syringomyelia. J Neurol 238:433–438 1991

    • Search Google Scholar
    • Export Citation
  • 10.

    Nishikawa MSakamoto HHakuba Aet al: Pathogenesis of Chiari malformation: a morphometric study of the posterior cranial fossa. J Neurosurg 86:40471997Nishikawa M Sakamoto H Hakuba A et al: Pathogenesis of Chiari malformation: a morphometric study of the posterior cranial fossa. J Neurosurg 86:40–47 1997

    • Search Google Scholar
    • Export Citation
  • 11.

    Nyland HKrogness KG: Size of the posterior fossa in Chiari type 1 malformation in adults. Acta Neurochir 40:2332421978Nyland H Krogness KG: Size of the posterior fossa in Chiari type 1 malformation in adults. Acta Neurochir 40:233–242 1978

    • Search Google Scholar
    • Export Citation
  • 12.

    Oldfield EHMuraszko KShawker THet al: Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. Implications for diagnosis and treatment. J Neurosurg 80:3151994Oldfield EH Muraszko K Shawker TH et al: Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. Implications for diagnosis and treatment. J Neurosurg 80:3–15 1994

    • Search Google Scholar
    • Export Citation
  • 13.

    Rhoton AL Jr: Microsurgery of syringomyelia and syringomyelic cord syndrome in Schmidek HHSweet WH (eds): Operative Neurosurgical Techniquesed 2. PhiladelphiaWB Saunders1988 pp 13071326Rhoton AL Jr: Microsurgery of syringomyelia and syringomyelic cord syndrome in Schmidek HH Sweet WH (eds): Operative Neurosurgical Techniques ed 2. Philadelphia WB Saunders 1988 pp 1307–1326

    • Search Google Scholar
    • Export Citation
  • 14.

    Sgouros SWilliams B: A critical appraisal of drainage in syringomyelia. J Neurosurg 82:1101995Sgouros S Williams B: A critical appraisal of drainage in syringomyelia. J Neurosurg 82:1–10 1995

    • Search Google Scholar
    • Export Citation
  • 15.

    Stovner LJBergan UNilsen Get al: Posterior cranial fossa dimensions in the Chiari I malformation: relation to pathogenesis and clinical presentation. Neuroradiology 35:1131181993Stovner LJ Bergan U Nilsen G et al: Posterior cranial fossa dimensions in the Chiari I malformation: relation to pathogenesis and clinical presentation. Neuroradiology 35:113–118 1993

    • Search Google Scholar
    • Export Citation
  • 16.

    Tachibana SIida HYada K: Significance of positive Queckenstedt test in patients with syringomyelia associated with Arnold-Chiari malformations. J Neurosurg 76:67711992Tachibana S Iida H Yada K: Significance of positive Queckenstedt test in patients with syringomyelia associated with Arnold-Chiari malformations. J Neurosurg 76:67–71 1992

    • Search Google Scholar
    • Export Citation
  • 17.

    Van Calenbergh FHoorens GVan Den Bergh R: Syringomyelia: a retrospective study Part II. Diagnostic and therapeutic approach. Acta Neurol Belg 90:1001101990Van Calenbergh F Hoorens G Van Den Bergh R: Syringomyelia: a retrospective study Part II. Diagnostic and therapeutic approach. Acta Neurol Belg 90:100–110 1990

    • Search Google Scholar
    • Export Citation
  • 18.

    Vega AQuintana FBerciano J: Basichondrocranium anomalies in adult Chiari type I malformation: a morphometric study. J Neurol Sci 99:1371451990Vega A Quintana F Berciano J: Basichondrocranium anomalies in adult Chiari type I malformation: a morphometric study. J Neurol Sci 99:137–145 1990

    • Search Google Scholar
    • Export Citation
  • 19.

    Williams B: The distending force in the production of “communicating syringomyelia.” Lancet 2:1891931969Williams B: The distending force in the production of “communicating syringomyelia.” Lancet 2:189–193 1969

    • Search Google Scholar
    • Export Citation
  • 20.

    Williams B: Simultaneous cerebral and spinal fluid pressure recordings. 2. Cerebrospinal dissociation with lesions at the foramen magnum. Acta Neurochir 59:1231421981Williams B: Simultaneous cerebral and spinal fluid pressure recordings. 2. Cerebrospinal dissociation with lesions at the foramen magnum. Acta Neurochir 59:123–142 1981

    • Search Google Scholar
    • Export Citation
  • 21.

    Williams B: Syringomyelia. Neurosurg Clin North Am 1:6536851990Williams B: Syringomyelia. Neurosurg Clin North Am 1:653–685 1990

    • Search Google Scholar
    • Export Citation

Cited By

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 314 314 10
Full Text Views 320 320 2
PDF Downloads 66 66 0
EPUB Downloads 0 0 0

PubMed

Google Scholar