MRI evidence for altered venous drainage and intracranial compliance in mild traumatic brain injury

Abstract

Purpose: To compare venous drainage patterns and associated intracranial hydrodynamics between subjects who experienced mild traumatic brain injury (mTBI) and age- and gender-matched controls.

Methods: Thirty adult subjects (15 with mTBI and 15 age- and gender-matched controls) were investigated using a 3T MR scanner. Time since trauma was 0.5 to 29 years (mean 11.4 years). A 2D-time-of-flight MR-venography of the upper neck was performed to visualize the cervical venous vasculature. Cerebral venous drainage through primary and secondary channels, and intracranial compliance index and pressure were derived using cine-phase contrast imaging of the cerebral arterial inflow, venous outflow, and the craniospinal CSF flow. The intracranial compliance index is the defined as the ratio of maximal intracranial volume and pressure changes during the cardiac cycle. MR estimated ICP was then obtained through the inverse relationship between compliance and ICP.

Results: Compared to the controls, subjects with mTBI demonstrated a significantly smaller percentage of venous outflow through internal jugular veins (60.9±21% vs. controls: 76.8±10%; p = 0.01) compensated by an increased drainage through secondary veins (12.3±10.9% vs. 5.5±3.3%; p<0.03). Mean intracranial compliance index was significantly lower in the mTBI cohort (5.8±1.4 vs. controls 8.4±1.9; p<0.0007). Consequently, MR estimate of intracranial pressure was significantly higher in the mTBI cohort (12.5±2.9 mmHg vs. 8.8±2.0 mmHg; p<0.0007).

Conclusions: mTBI is associated with increased venous drainage through secondary pathways. This reflects higher outflow impedance, which may explain the finding of reduced intracranial compliance. These results suggest that hemodynamic and hydrodynamic changes following mTBI persist even in the absence of clinical symptoms and abnormal findings in conventional MR imaging.

Figure 1. 3D Maximum Intensity Projected MR venography images demonstrating cerebral venous drainage patterns in a control subject (A) and in a subject with mTBI (B).

The internal jugular veins are well visualized in the control subject as the dominant outflow channel, while in the mTBI subject, the IJVs are not visualized and venous drainage occurs primarily through secondary veins, i.e., the epidural (filled arrows) and vertebral veins (empty arrow), which are well visualized.

Figure 2. Examples of high and low velocity encoded phase contrast images from a control subject (left) and a subject with mTBI (right).

A–B: Flow compensated magnitude images showing the bright signal from blood vessels. The augmented venous outflow through the epidural, vertebral veins (arrows) and the deep cervical veins (arrow heads) is well visualized. C–D: High-velocity encoding images used for measurements of arterial inflow and venous outflow through the jugular veins. E–F: Low-velocity encoding images used for measurements of the flow through the secondary channels (epidural, vertebral, and deep cervical veins) and the CSF flow. The lumen boundaries (red – arteries, blue- veins and yellow and red – CSF and cord) were identified using the PUBS automated segmentation method.

Figure 3. Derived volumetric flow waveforms obtained from a control subject (left) and a subject with mTBI (right).

The total arterial inflow (TCBF) and total venous flow though the jugular veins are shown in the top (Fig. 3A and 3B), respectively. The measured venous flow through the epidural, deep cervical, and vertebral veins are shown in the bottom (Fig. 3C and 3D).

Figure 4. Derived volumetric flow rates and intracranial volume change waveforms obtained from a control subject (left) and a subject with mTBI (right).

The arterial-minus-venous (A–V) and the CSF flow waveforms are shown in Fig. 4A and 4B. The Intracranial volume change during a cardiac cycle is shown in Fig. 4C and 4D, respectively. The CSF and the A–V waveforms are shown together to demonstrate the fact that the craniospinal CSF flow dynamics is driven by the net trans-cranial blood flow. The CSF waveform follows the A–V waveform more closely in the mTBI subject demonstrating the lower intracranial compliance compared to the matched control subject.