Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils

Implications for diagnosis and treatment

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✓ The mechanisms previously proposed for the progression of syringomyelia associated with Chiari I malformation of the cerebellar tonsils are controversial, leave many clinical observations unexplained, and underlie the prevalence of different operations currently used as initial treatment. To explore the mechanism of syringomyelia progression in this setting, the authors used anatomical and dynamic (phase-contrast and phase-contrast cine) magnetic resonance (MR) imaging, and intraoperative ultrasonography to examine the anatomy and dynamics of movement of the cerebellar tonsils, the wall of the spinal cord surrounding the syrinx, and the movement of cerebrospinal fluid (CSF) and syrinx fluid at rest, during the respiratory and cardiac cycles, and during Valsalva maneuver in seven affected patients.

In all patients the cerebellar tonsils occluded the subarachnoid space at the level of the foramen magnum. Syringomyelia extended from the cervical to the lower thoracic segment of the spinal cord. No patient had evidence of a patent communication between the fourth ventricle and the syrinx on anatomical MR images, dynamic MR images, or intraoperative ultrasound studies. Dynamic MR images of three patients revealed abrupt downward movement of the spinal CSF and the syrinx fluid during systole and upward movement during diastole, but limited movement of CSF across the foramen magnum during the cardiac cycle. Intraoperative ultrasound studies demonstrated abrupt downward movement of the cerebellar tonsils during systole that was synchronous with sudden constriction of the spinal cord and syrinx. Decompression of the foramen magnum was achieved via suboccipital craniectomy, laminectomy of C-1 and C-2, and dural grafting, leaving the arachnoid intact. Immediately after surgery, the pulsatile downward thrust of the tonsils and constriction of the spinal cord and syrinx disappeared. Syringomyelia resolved within 1 to 6 months after surgery in all patients.

Observations by the authors suggest the following previously unrecognized mechanism for progression of syringomyelia associated with occlusion of the subarachnoid space at the foramen magnum. The brain expands as it fills with blood during systole, imparting a systolic pressure wave to the intracranial CSF that is accommodated in normal subjects by sudden movement of CSF from the basal cisterns to the upper portion of the spinal canal. With obstruction to rapid movement of CSF at the foramen magnum, the cerebellar tonsils, which plug the subarachnoid space posteriorly, move downward with each systolic pulse, acting as a piston on the partially isolated spinal CSF and producing a systolic pressure wave in the spinal CSF that acts on the surface of the spinal cord. This causes progression of syringomyelia by abruptly compressing the cord and propelling the fluid in the syrinx longitudinally with each pulse, and may be responsible for the origin and maintenance of syringomyelia by the pulsatile pressure waves forcing CSF into the cord through the perivascular and interstitial spaces. Effective treatment occurs when the systolic pressure wave transmitted by the cerebellar tonsils is eliminated by relieving the obstruction to rapid movement of subarachnoid CSF across the foramen magnum. The presence of this mechanism can be detected preoperatively on dynamic MR images and during surgery on ultrasound studies by the pulsatile excursion of the wall of the spinal cord surrounding the syrinx and by its immediate disappearance and the expansion of the syrinx during forced inspiration after decompression of the tonsils. Effective treatment is achieved with bone and dural decompression of the foramen magnum alone, without entering the arachnoid.

Article Information

Address reprint requests to: Edward H. Oldfield, M.D., Surgical Neurology Branch, Building 10, Room 5D37, National Institutes of Health, 9000 Rockville Pike, Bethesda, Maryland 20892.

© AANS, except where prohibited by US copyright law.

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    Case 1. a: Sagittal T1-weighted magnetic resonance (MR) image of the cervical spine showing an inferior position of the cerebellar tonsils, obliteration of the subarachnoid space in the region of the foramen magnum, and syringomyelia extending to T-8. Web-like septa partially partition the syrinx. b and c: Phase-contrast MR images obtained at various points during the cardiac cycle. White areas indicate caudal flow and black areas cranial flow. The movement of the cerebrospinal fluid (CSF) and the syrinx fluid is cranial in the image (b) obtained 30 msec after the R wave of the electrocardiogram (EKG), when the brain capillaries contain the least amount of blood and before the aortic valve opens. Focal areas of high signal inside the syrinx, indicating caudal flow, are due to turbulence caused by septation in that cavity. The CSF and the syrinx fluid are moving caudally in the image (c) obtained 90 msec after the R wave of the EKG, when the brain expands due to arrival of blood into the capillary bed. The interval of cranially directed flow of subarachnoid spinal CSF (b) after the R wave was 9% of the R-to-R wave interval. Note the absence of upward movement of subarachnoid CSF across the foramen magnum during diastole (b) and limited downward flow during systole (c). After surgical correlation of the obstruction at the foramen magnum, the upward movement of subarachnoid CSF occupied 18% of the cardiac cycle after the R wave. d: Sagittal T1-weighted MR image of the cervical spine obtained 12 months after surgery. The syringomyelia has completely disappeared, the subarachnoid space at the foramen magnum is enlarged, and the partial obstruction is no longer present.

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    Case 3. a: Sagittal T1-weighted magnetic resonance (MR) image of the cervical spine revealing an inferior position of the cerebellar tonsils, marked narrowing of the subarachnoid space at the foramen magnum, and syringomyelia extending from C-1 to T12—L1. b and c: Phase-contrast MR images demonstrating bidirectional flow of cerebrospinal fluid (CSF) and syrinx fluid during the cardiac cycle. White areas indicate caudal flow and black areas cranial flow. In the image (b) obtained before the arrival of blood in the brain capillaries, the flow of spinal CSF after the R wave is cranial occurring for the initial 10% of the R-to-R wave interval. In the image (c) obtained during midsystole, the expansion of the brain has reversed the CSF flow to a caudal direction. Note the absence of movement of subarachnoid CSF after the foramen magnum during diastole (b) and minimal movement during systole (c). d: Sagittal T1-weighted MR image obtained 14 months after surgery. The cavity in the cord has collapsed, the subarachnoid space anterior and posterior to the cord at the level of the foramen magnum is much larger than before surgery, and the anatomical correction provided by surgical decompression now permits unimpeded bidirectional flow of CSF at this level. After surgical correction of the obstruction at the foramen magnum, the duration of upward flow of CSF after the R wave was longer, occupying 25% of the cardiac cycle.

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    Schematic drawings of the foramen magnum region, sagittal view, illustrating the proposed mechanism of origin and progression of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. a: In normal subjects during systole (right), as the brain expands With the reception of blood, cerebrospinal fluid (CSF) moves from the fourth ventricle into the cisterna magna; a larger volume of fluid passes from the basal cisterns to the subarachnoid space of the upper portion of the spinal canal. The magnitude of the systolic pressure wave that is conveyed to the CSF in the spinal canal dissipates with increasing distance inferiorly. During diastole (left), CSF flows rostrally across the foramen magnum. b: With obstruction to the rapid to-and-fro movement of CSF in the subarachnoid space across the foramen magnum (ventrally by anterior displacement of the brain stem and posteriorly by the impacted cerebellar tonsils) during systole (center) and diastole (left), brain expansion during systole is accommodated by abrupt caudal movement of the tonsils. The piston-like effect of this movement on the partially isolated spinal subarachnoid space imparts an accentuated systolic pressure wave to the spinal subarachnoid CSF. This acts on the surface of the upper segments of the spinal cord, abruptly constricting the syrinx, propelling the fluid in it inferiorly and increasing bulk movement of CSF into the cord. In some patients an inferior position of the foramen of Magendie may deposit CSF expelled from the fourth ventricle during systole into the spinal canal below the level of obstruction (right). c: With surgical decompression of the foramen magnum and tonsils, occlusion of CSF flow across the foramen magnum is eliminated, normal physiology is restored, and syringomyelia disappears.

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