By Mark Luciano, MD, PhD; Bryn Martin, PhD; Phil Allen, PhD; and Francis Loth, PhD
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In children and adults, Chiari malformation is recognized as a disorder of the cervical-medullary junction that consists of crowding and compression at the foramen magnum (Figure 1).
Figure 1. Type 1 Chiari malformation and associated spinal cord syrinx in a 7-year-old patient, imaged using T2-weighted sagittal MRI.
The current radiographic criterion for the diagnosis of Chiari is cerebellar tonsillar descent below the foramen magnum greater than 3 to 5 mm. Because of the complexity of the region compressed, Chiari may present with a variety of symptoms including headache, cranial nerve dysfunction or extremity deficits. This variable presentation results in a large differential diagnosis and great potential for misdiagnosis.
While Chiari crowding may occur in 1 to 3 percent of the population, symptoms may occur in only 0.06 percent.1 The poor correlation between the extent of cerebellar crowding and symptoms has led medical scientists to seek other features beyond the static anatomical picture seen on MRI to predict symptoms and guide surgical treatment.
Fluid Motion and Symptoms
Cerebrospinal fluid (CSF), blood and brain tissue all move in the cervical-medullary junction with each heartbeat. Abnormal motion of these fluids and tissues has been suspected to be an important factor contributing to hindbrain descent, compression and ultimately symptoms.
Understanding the effect that abnormal motion has on Chiari symptoms requires a multidisciplinary approach. For this reason, Cleveland Clinic clinicians in pediatric and congenital neurosurgery, radiological physicists and pain specialists are working closely with a team of neuroscientists, engineers and psychologists at the Conquer Chiari Research Center at the University of Akron. This multidisciplinary approach has yielded novel results that have changed our thinking about Chiari diagnosis and treatment and inspired new questions.
The connection between CSF motion and brain tissue damage is not a new idea. The importance of a repetitive “water hammer effect” acting on the cerebellum, brain stem and spinal cord was first postulated in 19653 by W. James Gardner, MD, Cleveland Clinic’s first Chairman of Neurosurgery. The “Gardner hypothesis” has been greatly debated and has influenced the diagnostic and surgical approach to Chiari for decades.
Novel Imaging Methods
Since that time, novel MRI-based techniques such as 3-D assessment of CSF motion have been developed (Figure 2a).4
Figure 2a. 3-D measurement of CSF flow velocities by 4-D phase-contrast MRI4 in a 5-year-old Chiari patient with mild tonsillar descent, showing regions of elevated CSF flow velocities on the anterior side of the spinal cord from the pontine cistern (image courtesy of Alexander Bunck, MD).
Researchers have used computational fluid dynamics to model the dynamic nature of CSF in unprecedented detail (Figure 2b) and have shown that Chiari patients exhibit greater CSF flow impedance than do controls.2,5
Figure 2b. Subject-specific computational fluid dynamics simulation of CSF motion based on in vivo MRI measurements from an adult-age Chiari patient with mild tonsillar descent below the foramen magnum7 (figure left = posterior CSF space, right = anterior; arrows show direction and magnitude of velocity streamlines). (Image courtesy of Soroush Pahlavian, MS.)
While decompressive surgery may open the fluid spaces at the foramen magnum, the effect on impedance is variable. Clinicians are now asking if the variable postsurgical course of Chiari sufferers is related to CSF flow impedance or other engineering-based parameters.
Since Dr. Gardner’s time, it has been suspected that cardiac-driven CSF flow and its associated forces act on neural tissues to deform the cerebellum, brain stem and spinal cord. Clinicians have long noted pulsatile movement of the cerebellar tonsils via intraoperative ultrasound imaging.
Using novel phase-contrast MRI-based techniques, our group has observed an increase in neural tissue motion in Chiari patients versus controls and has shown that motion often decreases after surgical decompression (Figure 3). Interestingly, the pattern of cyclic tissue compression and stretching also showed differences for Chiari patients. Understanding the tissue stresses due to the repetitive microstretching of the hindbrain may shed more light on the symptoms and neural tissue damage in Chiari.
Figure 3. Quantification of spinal cord bulk motion at the foramen magnum using phase-contrast MRI, showing greater motion in Chiari (CM) patients than in healthy subjects, and that motion decreased following surgery.
Cognitive and Emotional Changes
Finally, although Chiari compromises a region not often associated with influence on higher brain function, recent findings of our multidisciplinary group have suggested there are changes in cognitive and emotional control in some Chiari patients.6 While this clinically important change may be due partially to the nonspecific result of chronic pain, there was evidence of cognitive effects that appeared to be independent of pain.
Our team is now investigating the possibility of a Chiari-specific origin of these cognitive effects by examining the association between Chiari brain compression and both fiber injury and abnormal higher brain region function, using diffusion tensor imaging and functional MRI, respectively.
The multidisciplinary collaboration at Cleveland Clinic and the University of Akron has resulted in new ways of quantifying and understanding the underlying pathophysiology of Chiari. Determining how this new information can inform the diagnosis and surgical treatment of pediatric and adult Chiari patients is the priority of this joint venture.
- Speer MC, Enterline DS, Mehltretter L, Hammock P, et al. Review article: Chiari type I malformation with or without syringomyelia: Prevalence and genetics. J Genet Couns. 2003;12:297-311.
- Martin BA, Kalata W, Shaffer N, Fischer P, Luciano M, Loth F. Hydrodynamic and longitudinal impedance analysis of cerebrospinal fluid dynamics at the craniovertebral junction in type I Chiari malformation. PLoS One. 2013;8(10):e75335.
- Gardner, WJ. Hydrodynamic mechanism of syringomyelia: Its relationship to myelocele. J Neurol Neurosurg Psychiatry. 1965;28:247-259.
- Yiallourou TI, Kröger JR, Stergiopulos N, Maintz D, Martin BA, Bunck AC. Comparison of 4D phase-contrast MRI flow measurements to computational fluid dynamics simulations of cerebrospinal fluid motion in the cervical spine. PLoS One. 2012;7(12):e52284.
- Shaffer N, Martin BA, Rocque B, et al. Cerebrospinal fluid flow impedance is elevated in Type I Chiari malformation. J Biomech Eng. 2014;136(2):021012.
- Allen PA, Houston JR, Pollock JW, et al. Task-specific and general cognitive effects in Chiari malformation type I. PLoS One. 2014;9(4):e94844.
- Heidari Pahlavian S, Yiallourou T, Tubbs RS, Bunck AC, Loth F, et al. The impact of spinal cord nerve roots and denticulate ligaments on cerebrospinal fluid dynamics in the cervical spine. PLoS One. 2014;9(4):e91888.
Dr. Luciano is a staff pediatric and adult neurosurgeon, Head of Pediatric and Congenital Neurosurgery, and Director of the CSF Physiology Laboratory at Cleveland Clinic, with adjunct positions in biomedical engineering at Cleveland Clinic and Cleveland State University. His specialty interests include general pediatric neurosurgery, congenital anomalies, transitional neurosurgery and CSF disorders.
Dr. Martin is a research assistant professor in the Department of Mechanical Engineering at the University of Akron and Director of the Conquer Chiari Research Center. His specialty interest is the pathophysiology of CSF system disorders with focuses on Chiari malformation, syringomyelia and hydrocephalus.
Dr. Allen is a professor of psychology at the University of Akron. His specialty interest in Chiari malformation type I concerns how cognition and emotion are related to the systems neuroscience of this disorder.
Dr. Loth is a professor and holds the F. Theodore Harrington Endowed Chair in the Department of Mechanical Engineering at the University of Akron. He also is executive director of the Conquer Chiari Research Center. His specialty interest is the simulation and measurement of blood and cerebrospinal fluid dynamics.