Traffic and cargo on the venous highway: distribution of venous flow and oxygenation in the human brain.
Jill B. De Vis1, Hanzhang Lu2, Harshan Ravi2, Jeroen Hendrikse1, and Peiying Liu3

1Radiology, University Medical Center Utrecht, Utrecht, Netherlands, 2Radiology, Johns Hopkins University School of Medicine, Baltimore, MD, United States, 3Radiology, Johns Hopkins University Medical Center, Baltimore, MD, United States

Synopsis

Arterial territory and flow have been well studied, but few studies have been performed to investigate the venous flow distribution. Similarly, little is known about the oxygenation and its heterogeneity among the different venous structures. The purpose of this study was to investigate venous flow distribution and oxygenation.

Introduction

The brain’s arterial flow and flow territories have been well investigated, while little is known about the venous system. There have been only occasional reports in literature that assessed cerebral blood flow variation in trajectories of the venous system1. Similarly, studies investigating the venous oxygenation (Yv) are scarce due to a lack of tools for in vivo quantification of this parameter2. Therefore the purpose of this study was to investigate the distributions of venous flow and oxygenation in the brain, and understand how they might change under challenged state. For this purpose, we measured the blood flow and oxygenation at the major veins in the brain’s drainage system under both baseline and physiological challenge conditions with hypercapnia and hyperoxia.

Methods

Study design:

Eight subjects (4 males, 24-37yrs) were studied on a Philips 3T scanner. The study contained two parts: 1) Measurement of venous blood flow at major veins, specifically superior sagittal sinus (SSS), straight sinus (SS) and internal jugular veins (IJVs), using phase-contrast (PC) MRI during both room air and hypercapnia (5% CO2) breathing; 2) Measurement of venous oxygenation in these veins using T2-relaxation-under-spin-tagging (TRUST) MRI3 under both room air and hyperoxia (95%O2) breathing.

Venous flow measurements:

For each subject, a 3D time-of-flight angiogram and venogram was performed first to visualize the brain’s feeding arteries and major draining veins. For reference, whole-brain arterial blood flow was calculated as the sum of flux measured at the four feeding arteries, left and right internal carotid arteries (ICAs) and left and right vertebral arteries (VAs). Venous flow was measured in SSS, SS and IJVs. The PC-MRI imaging parameters used those optimized in a recent study4. Manual ROI drawing was used to quantify the blood flux (in ml/min) in each vessel.

Venous oxygenation measurements:

TRUST MRI is based on the principle that T2 relaxation time of the blood has a well-known and calibratable relationship with its oxygenation. The scan duration of TRUST MRI was 1 min 12 sec and its imaging protocol and analysis followed that of a recent multi-site trial5.

Results

Venous flow distribution:

Results of the blood flow measurements are shown in Table 1. The venous drainage distribution was illustrated in Figure 1a. We found that the venous blood drained from the cortex (i.e., flow through SSS) and that drained from deep brain structures (i.e., flow through SS) comprised around 62% of the whole-brain blood (i.e., total arterial inflow). Since the IJVs drain about 76% of the whole-brain blood, it means the cerebellar veins and other small veins joining the venous sinuses after the sinus confluence contribute about 14% of the total blood. Moreover, about 24% of cerebral blood was not drained by the IJVs, but via venous plexuses which consequently drain into the cervical veins and external jugular veins. The drainage distribution did not change significantly during hypercapnia.

Venous oxygenation distribution:

The measured Yv at baseline was 61±4%, 64±4%, and 62±4% in SSS, SS, and IJVs respectively (Figure 1b). The SS-Yv was significantly higher than SSS-Yv (p=0.0003, Figure 2a). Since the blood in the IJV is originated predominantly from SSS and SS, not surprisingly the IJV-Yv value is between that of SSS and SS. There was significant correlation between SSS-Yv and SS-Yv (R2=0.88, Figure 2b), and between SSS-Yv and IJV-Yv (R2=0.65). The Yv at hyperoxia was 70±3%, 71±5%, and 68±5% in SSS, SS, and IJVs respectively. No significant difference in hyperoxia-induced Yv change was detected among the major veins.

Discussion

In this work we evaluated the distribution of flow and oxygenation in the venous drainage system of the brain. Remarkably, about 24% of the venous blood is not drained via the commonly assumed pathway, i.e. the cerebral venous sinuses. We also found that although the oxygenation is slightly higher in SS which drains deep brain structure, the oxygenation in IJVs, which reflects whole brain venous oxygenation, is correlated and mainly driven by cortical venous oxygenation. Therefore, if one wants to know the whole-brain oxygenation consumption, Yv measurements on the SSS are sufficient. Caution should be taken in case of disease conditions in which oxygen consumption in the deep gray matter or cerebellum differs considerably from the rest of the brain, e.g. ischemia within these areas. In this case, additional Yv measurements on the SS and IJVs by TRUST MRI can be considered.

Acknowledgements

No acknowledgement found.

References

1. Schuchardt et al., Eur Radiol 2015;25(80:2371-80.

2. Krishnamurthy et al., MRM 2014;71(3):978-89.

3. Lu et al., MRM 2008;60(2):357-63.

4. Peng et al., JMRI 2015;42(4):1126-33.

5. Liu P et al., Magn Reson Med 2015;doi:10.1002/mrm.25627.

Figures

Table 1. Blood flow at baseline and hypercapnia.

HC, hypercapnia; ΔHC, the percentage flow change from baseline to hypercapnia; AI, arterial inflow, flow through the 4 brain feeding arteries; SSS, superior sagittal sinus; SS, straight sinus; IJVs, internal jugular veins.


Figure 1: Blood flow and oxygenation in the venous system.

(a) Pie plot of the venous blood distribution. (b) Illustration of the blood flow (normalized by whole-brain blood flow) and oxygenation (in units of oxygen saturation fraction) in the venous drainage system.

CBF, cerebral blood flow; CVs, cerebellar veins and other small veins joining the venous sinuses after the confluence; SS, straight sinus; SSS, superior sagittal sinus; Yv, venous oxygenation.


Figure 2: Results of the venous oxygenation measurements. (a) Yv at the major veins. (b) Scatter plot between SSS-Yv and SS-Yv. Red line indicates unity line.

IJV, internal jugular veins; SS, straights sinus; SSS, superior sagittal sinus; Yv, venous oxygenation.




Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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