Study on the Interaction Between Cerebral Blood Flow and Cerebrospinal Fluid Dynamics Measured at Intracranial and Extracranial Planes

Background

The interaction between cerebral blood flow (CBF) and cerebrospinal fluid (CSF) is a critical factor in maintaining intracranial pressure (ICP) stability. According to the Monro-Kellie doctrine, the intracranial volume (including brain parenchyma, CSF, and blood) is constant, and any changes in one compartment must be compensated by the others. However, recent studies have shown that the dynamic changes in CBF and CSF do not fully adhere to this doctrine, especially during the cardiac cycle, where minor changes in CBF may not be entirely balanced by CSF. This phenomenon is significant in various neurological disorders, such as hydrocephalus and Alzheimer’s disease.

Although many studies have measured the dynamic changes in CBF and CSF using phase-contrast magnetic resonance imaging (PC-MRI), most have focused on extracranial planes (e.g., carotid arteries and internal jugular veins). However, the anatomical structure and hemodynamics of extracranial veins exhibit significant individual variability, which may affect the accuracy of measurements. Therefore, this study aims to compare the differences in measuring the interaction between CBF and CSF dynamics at intracranial and extracranial planes and to determine which plane is more suitable for studying their interaction.

Source of the Paper

This paper was co-authored by Kimi Piedad Owashi, Pan Liu, Serge Metanbou, Cyrille Capel, and Olivier Balédent, affiliated with the Medical Image Processing Department, Radiology Department, and Neurosurgery Department of Amiens-Picardie University Hospital in France. The paper was published in 2024 in the journal Fluids and Barriers of the CNS under the title “Phase-contrast MRI analysis of cerebral blood and CSF flow dynamic interactions.”

Research Process and Results

1. Study Population and Experimental Design

The study included 38 healthy young volunteers (18 females, 20 males) aged 19 to 35 years. All participants had no history of neurological, psychiatric, or other severe diseases. Data were collected using a 3T MRI system, primarily measuring CBF at intracranial and extracranial planes and CSF flow at the C2-C3 level.

2. Data Acquisition and Processing

The study used PC-MRI to measure the dynamic changes in CBF and CSF. The intracranial plane measured blood flow in the left and right internal carotid arteries, basilar artery, straight sinus, and superior sagittal sinus, while the extracranial plane measured blood flow in the left and right internal carotid arteries, left and right vertebral arteries, and left and right internal jugular veins. CSF flow was measured at the C2-C3 level.

Data were processed using in-house software “Flow,” which employs a semi-automatic segmentation algorithm to correct eddy current effects and calculate dynamic flow rates of CBF and CSF. By integrating the flow rate curves of CBF and CSF, the study calculated cerebral blood volume change (CB_VC) and cerebrospinal fluid volume change (CSF_VC).

3. Key Findings

The study found that the amplitude of CB_VC was significantly higher at the extracranial plane (0.89 ± 0.28 ml/cc) compared to the intracranial plane (0.73 ± 0.19 ml/cc; p < 0.001). Additionally, the linear relationship between CB_VC and CSF_VC was stronger at the intracranial plane (R²: 0.82 ± 0.16; slope: -0.74 ± 0.19) compared to the extracranial plane (R²: 0.47 ± 0.37; slope: -0.36 ± 0.33; p < 0.001). This indicates that measurements at the intracranial plane better reflect the interaction between CBF and CSF.

4. Conclusions and Significance

The results suggest that CSF does not fully balance CBF changes during the cardiac cycle, which differs from the expectations of the Monro-Kellie doctrine. Furthermore, CBF measurements at the intracranial plane show a stronger correlation with CSF dynamics, indicating that the intracranial plane is more suitable for studying the interaction between CBF and CSF. This finding provides new insights for future research on ICP changes and related neurological disorders.

Highlights of the Study

1. First Intracranial Plane Measurement of CBF: This study is the first to measure CBF below the circle of Willis, validating the dynamic relationship between CSF and CBF.
2. Comparison of Intracranial and Extracranial Planes: By comparing measurements at intracranial and extracranial planes, the study revealed the impact of individual variability in extracranial venous anatomy and hemodynamics on measurement accuracy.
3. Application of In-House Software: The study used the in-house software “Flow” for data processing, improving the accuracy of CBF and CSF flow measurements.

Other Valuable Information

The study also found significant individual variability in extracranial venous hemodynamics, which may be related to anatomical variations in the internal jugular veins. Additionally, the study suggested that future research should consider the impact of cardiac cycle length on CBF and CSF dynamics.

Summary

This study, using PC-MRI, is the first to measure CBF at the intracranial plane, revealing the dynamic relationship between CSF and CBF. The results indicate that the intracranial plane is more suitable for studying the interaction between CBF and CSF, providing new perspectives for future research on ICP changes and related neurological disorders.