Measuring Cerebrospinal Fluid Flow and Brain Motion After Surgery in People with Chiari Malformations Type 1

Introduction::
Chiari Malformation I (CM-1) is defined as a herniation of the cerebellar tonsil through the foramen magnum of greater than 5mm (Figure 1A)¹. Individuals with CM-1 often have headaches, paresthesia, nausea, dysphagia, and sleep apnea^2,3. It is observed that CM-1 causes a disruption in cerebrospinal fluid (CSF) exchange between the skull and spinal cord. This is commonly attributed to a narrowing of the CSF channel, but we believe that changes to the normal pulsatile brain motion from the cardiac cycle are additionally contribute to CSF flow disruptions⁴.




In some CM-1 cases, posterior fossa decompression surgery is recommended to alleviate symptoms, which involves removal of a section of bone at the base of the skull⁵ (Figure 1B). However, determining which patients are the best candidates for surgery can be challenging. Some individuals have large tonsillar decent ( >10mm) without clinical symptoms, as they may have a large foramen magnum opening or normal brain motion, while others have small tonsillar descents (~5mm) with severe clinical symptoms⁶. Therefore, the ability to quantitively measure the secondary effects of tonsillar decent, including changes to CSF flow and pulsatile brain motion, can help categorize which individuals are likely to have positive surgical outcomes.




Novel MRI sequences only recently allows us to quantify CSF flow, using phase-contrast magnetic resonance (PCMR) imaging, and brain motion using DENSE, which was originally developed to measure cardiac motion. This work is the first-time the relationship between brain motion and CSF flow has been quantitively measured in CM-1 before and after surgery.




Materials and Methods::
84 people (ages 18-71) with a clinical diagnosis of CM-1 participated in this study. 36 subjects had posterior fossa decompression surgery and participated in a second MRI 3-months after surgery. Participants were scanned on a Siemens 3T Prisma MRI with a 32-channel head coil. Retrospectively ECG-gated, 2D axial PCMR images were acquired (FOV=220x220, resolution=1.15x1.15x5 mm, TE/TR=6/21ms). For each cardiac cycle 25 temporal images with 2 segments and 2 averages were collected. CSF flow was calculated as a function of time using manually drawn regions-of-interest in Segment (Medviso). Segment integrates pixel-wise velocity and outputs an average flow at each time-point across one cardiac cycle. Stoke volume was calculated as the average of the absolute value of forward and backward flow.




DENSE scans were acquired at the midline in the sagittal orientation using a two-dimensional spiral cine technique with peripherally pulse unit-gating. DENSE data was acquired with displacement encoding in the anterior-posterior (x) direction and superior-inferior (y) direction. DENSE acquisitions were initialized with a tagging pulse at the peak of the peripheral pulse unit signal, and a total of 13– 29 frames were acquired over the cardiac cycle depending on the subject’s heart rate⁷. Parameters included: flip angle = 15 degrees, temporal resolution = 34ms, encoding frequency = 0.6 cycles/mm, interleaves per heartbeat = 2, FOV = 256×256, pixel size = 0.94 × 0.94 mm, and slice thickness = 8 mm. Sagittal high-resolution T₁- and T₂-weighted anatomical scans were also acquired to assess severity of tonsillar decent.




Results, Conclusions, and Discussions::
CSF stroke volume in untreated CM-1 was on average 0.859 ± 0.58ml per cardiac cycle, whereas surgical intervention showed CSF flow of 1.141 ± 0.43ml per cardiac cycle (p=0.036; Figure 2). Pairwise pre- to post-surgical saw CSF stroke volume improve 40.5% with a significance of p=0.011. We did not observe a significant change in peak maximum velocity after surgery (5.81cm/s vs. 5.51cm/s; p=0.178).




Interestingly, we also saw that brainstem motion decreases after decompression surgery. Average brainstem motion in CM-1 patients was 187.2µm without intervention, after intervention, motion was 161.8µm (p=0.065). As expected, this motion was larger in the y-direction (superior-to-inferior), 180.4µm displacement with no intervention to 153.9µm displacement with intervention (p=0.038); x-direction motion was 86.4µm with no intervention and 78.9µm (p=0.356) with intervention (Figure 3). On a pairwise basis, subjects showed a 17.3% decrease in total brain motion after surgery (p=0.007), with a maximum change in motion of any subject being 55.9%. Based on previous literature, brain motion is elevated pre-surgery and returns to normal after surgery⁸. Elevated brain motion in CM-1 is likely due to higher cerebral pressure gradients which occur with the cardiac cycle.




The Monroe Kelly doctrine describes that CSF volume in the skull is inverse to volume of blood. The pressure differences from the cardiac blood fluxuations in the brain, expands and contracts cerebral tissue, and acts as a pump for CSF flow⁹. Here, we find a positive correlation between the magnitude of change in brain motion and the magnitude of change in CSF flow (R=0.462; p=0.020; Figure 4). These changes were not related to degree of tonsillar decent (p=0.417), indicating that this metric alone is insufficient for describing surgical outcomes.









Conclusion




CM-1 is a prevalent disorder which affects 1 in 1000 individuals, but only some cases result in severe impacts on quality of life. Deciding if surgical intervention is valuable can be challenging. Here, we present quantitative MRI techniques for characterizing the physiological cascade resulting from tonsillar decent. We expect that these quantitative metrics will be valuable in surgical planning and ultimately improve patient outcomes.




Acknowledgements (Optional): : This research was supported by Conquer Chiari.

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