Long-term recovery behavior of brain tissue in hydrocephalus patients after shunting

Abstract

The unpredictable complexities in hydrocephalus shunt outcomes may be related to the recovery behavior of brain tissue after shunting. The simulated cerebrospinal fluid (CSF) velocity and intracranial pressure (ICP) over 15 months after shunting were validated by experimental data. The mean strain and creep of the brain had notable changes after shunting and their trends were monotonic. The highest stiffness of the hydrocephalic brain was in the first consolidation phase (between pre-shunting to 1 month after shunting). The viscous component overcame and damped the input load in the third consolidation phase (after the fifteenth month) and changes in brain volume were stopped. The long-intracranial elastance (long-IE) changed oscillatory after shunting and there was not a linear relationship between long-IE and ICP. We showed the long-term effect of the viscous component on brain recovery behavior of hydrocephalic brain. The results shed light on the brain recovery mechanism after shunting and the mechanisms for shunt failure.

Fig. 1. Computer simulation and data validation.

a 3-D models of the outer layer of subarachnoid space and ventricular system (not to scale) for patient No. 1 before shunting. b Meshed models of brain and ventricular system (not to scale) for patient No. 1 fifteen months after shunting. c meshed model of the head substructure for patient No. 1 fifteen months after shunting. Turquoise and purple areas represent the fluid domain (CSF space: ventricular system and subarachnoid) and solid domain (brain), respectively. The borders and interfaces between turquoise and purple areas are the FSI boundaries. d The FSI simulation results for ICP and force for patient No. 1 before shunting. e Grid independence study. f Validation of the maximum CSF velocity in the cerebral aqueduct and maximum ICP which were measured using FSI simulation. Raw data for panel f is included in Supplementary Table 1. CSF cerebrospinal fluid, ICP intracranial pressure, FSI fluid-structure interaction, Cine-PC MRI cine phase-contrast magnetic resonance imaging.

Fig. 2. Changes in volumes of CSF and brain, ICP, and force after shunting.

a Mean CSF volume and CSF volumes of all patients before shunting until 15 months after shunting. b Mean brain volume and brain volumes of all patients before shunting until 15 months after shunting. c Mean ICP and ICPs of all patients before shunting until 15 months after shunting. d Mean force and forces in all patients before shunting until 15 months after shunting. It should be noted that the mean volumes, ICP, and force for healthy subjects also showed on the left side panels. The gray areas in statistical analysis tables show the stable areas of volumes, ICP, and fore changes. The CSF volume, brain volume, ICP, and forces values reached stable conditions 12, 15, 6, and 9 months after shunting, respectively. Since the differences between the values of these parameters in stable months were less than 1.0%. Hence, follow-up was stopped 15 months after shunting, and results were reported until the fifteenth month. Raw data for Fig. 2 is included in Supplementary Data 1. CSF cerebrospinal fluid, ICP intracranial pressure, SD standard deviation, SE standard error, CV coefficient of variation, CI confidence of interval.

Fig. 3. Changes in strain and creep of CSF and brain after shunting.

a Mean CSF and brain strain. b CSF and brain strain of all patients until 15 after shunting. c Mean CSF and brain creep. d CSF and brain creep of all patients until 15 after shunting. CSF volume changes after the twelfth month were negligible, hence, CSF strain and creep values after the twelfth month were not calculated. The reason for the negative values of CSF strain is the descending trend of CSF volume changes after shunting. “Stages 1–2” means the CSF volumetric creep between the first and second months after shunting. Raw data for Fig. 3 is included in Supplementary Tables 2–5. CSF Cerebrospinal fluid.

Fig. 4. Changes in brain stiffness and elastance after shunting.

a shows the changes in the force exerted by CSF on the brain material versus brain volume. b and c show the stiffness and mean stiffness changes in hydrocephalic brains after shunting, respectively. Force changes after the ninth month were negligible, hence, body force versus brain volume and consequently stiffness after the ninth month were not calculated in (b) and (c). d changes of ICP versus CSF volume for all patients after shunting. e and f are mean IE and IEs of all patients after shunting, respectively. ICP changes after the sixth month were negligible, hence, IE values after the sixth month were not calculated. “Stages 0–1” means the IE is calculated between before shunting to 1 month after shunting. g shows the results of the Pearson correlation coefficient for assessing the relationship between ICP and CSF volumes in all patients. P-values for all patients were higher than 0.23 and non-significant. Raw data for Fig. 4a–f are included in Supplementary Data 1, Supplementary Table 6, Supplementary Table 6, Supplementary Data 1, Supplementary Table 7, and Supplementary Table 7, respectively. Raw data for Fig. 4g is included in Supplementary Table 7 and Supplementary Data 1. CSF cerebrospinal fluid, ICP intracranial pressure, IE intracranial elastance.

Fig. 5. Changes in ICP, CSF volume, and time concurrently.

The changes in CSF volume and brain volume with respect to time (months after shunting). The plans show the concurrent changes in volumes after shunting. Raw data for Fig. 5 is included in Supplementary Table. CSF cerebrospinal fluid.

Fig. 6. Methodological workflow.

The workflow included FSI method (blue text), measured parameters (green text), and calculated parameters (maroon text).