NEUROSURGICAL FOCUS Neurosurg Focus 41 (3):E9, 2016 Cerebral venous overdrainage: an under-recognized complication of cerebrospinal fluid diversion Kaveh Barami, MD, PhD Department of Neurosurgery, Kaiser Permanente Northern California, Sacramento, California Understanding the altered physiology following cerebrospinal fluid (CSF) diversion in the setting of adult hydrocephalus is important for optimizing patient care and avoiding complications. There is mounting evidence that the cerebral venous system plays a major role in intracranial pressure (ICP) dynamics especially when one takes into account the effects of postural changes, atmospheric pressure, and gravity on the craniospinal axis as a whole. An evolved mechanism acting at the cortical bridging veins, known as the “Starling resistor,” prevents overdrainage of cranial venous blood with upright positioning. This protective mechanism can become nonfunctional after CSF diversion, which can result in posture- related cerebral venous overdrainage through the cranial venous outflow tracts, leading to pathological states. This review article summarizes the relevant anatomical and physiological bases of the relationship between the craniospinal venous and CSF compartments and surveys complications that may be explained by the cerebral venous overdrainage phenomenon. It is hoped that this article adds a new dimension to our therapeutic methods, stimulates further research into this field, and ultimately improves our care of these patients. http://thejns.org/doi/abs/10.3171/2016.6.FOCUS16172 KEY WORDS cerebrospinal fluid diversion; hydrocephalus; posture; shunt; Starling resistor; cerebral venous overdrainage HE intimate relationship between cerebral venous ent pressure (CSF in the subarachnoid space) all contained and cerebrospinal fluid (CSF) compartments is in a rigid box, such as the skull in the hydraulic model increasingly recognized as an important aspect of shown in Fig. 1. The Starling resistor is a site of compres- Tintracranial pressure (ICP) dynamics when one considers sion, also known as a “choke point,” at the junction be- the craniospinal axis and the effects of gravity and atmo- tween the bridging vein and the sagittal sinus such that spheric pressure on it as a whole.5 From an evolutionary when pressure in the superior sagittal sinus drops during standpoint, as we became bipedal, certain accommodat- upright posture, the higher CSF pressure will choke the ing mechanisms developed to prevent during upright po- downstream connection to the sagittal sinus and prevent sitioning the overdrainage of fluid (CSF or blood) from venous overdrainage.50 Concurrently pressure in the cere- the cranial to the spinal compartment, which could lead to bral veins proximal to the Starling resistor is maintained intracranial hypotension.18,50,75,92,95 at a higher level than CSF pressure because of the created One such mechanism known as the “Starling resistor,” back pressure.39,44 Thus the Starling resistor is responsible which has been conserved across species,50 acts at the for maintaining the hierarchy of pressures of the various junction between cortical bridging veins that drain into liquid compartments in the cerebrum, that is, arterial in- the superior sagittal sinus, prevents siphoning of venous flow pressure > cerebral venous pressure > subarachnoid blood, and maintains ICP as we stand up.34,47,48 As the col- CSF pressure > sagittal sinus pressure. This, in turn, cre- lapsible cortical bridging veins are draining into the rigid ates a pressure gradient to promote CSF drainage into the venous sinuses, they traverse the subarachnoid space and sagittal sinus. Various anatomical and MRI studies of the are subject to surrounding external CSF pressure. Essen- terminal regions of bridging veins are consistent with the tially, the Starling resistor is a mechanism that maintains idea that the Starling resistor functions as a flow resis- constant flow through collapsible tubes (such as cortical tor.64,68,80,88 draining veins) when they are surrounded by variant ambi- Several studies have shown that there are predictable ABBREVIATIONS CSF = cerebrospinal fluid; ICP = intracranial pressure. SUBMITTED April 10, 2016. ACCEPTED June 16, 2016. INCLUDE WHEN CITING DOI: 10.3171/2016.6.FOCUS16172. ©AANS, 2016 Neurosurg Focus Volume 41 • September 2016 1 Unauthenticated | Downloaded 09/26/21 05:11 PM UTC K. Barami FIG. 1. Schematic of the hierarchy of pressures of various liquid components of the intracranial space. Arrows indicate the Starling resistor at the lateral lacunes (the junction between the cortical bridging vein and the sagittal sinus). Arterial inflow pressure (Pa) is higher than CSF pressure (Pcsf), which in turn is higher than pressure in the superior sagittal sinus (Pss). Pressure in the upstream cerebral veins (Pcv) is always maintained above Pcsf because of the constriction effect by the Starling resistor; this phenomenon also prevents venous overdrainage during upright positioning when sagittal sinus pressure falls. From Luce et al: J Appl Physiol 53:1496–1503, 1982. Published with permission. changes in ICP and cerebral venous pressure with altera- tion, because of atmospheric pressure, the internal jugular tions in body posture.15,27 Intracranial pressure studies at veins collapse and venous blood is rerouted to nonjugular different tilt angles have shown that there is a faster re- pathways, specifically to the noncollapsible vertebral ve- duction of ICP at smaller angles and a slower reduction at nous plexus.28,82 In a systematic ultrasonography and MRI higher angles.2,8,73 In healthy subjects, with upright posture analysis of the types and prevalence of human cerebral there is a drop in ICP ranging between -5 and 5 cm H2O venous outflow, it was shown that there is predominantly with reference to the foramen magnum. The drop in ICP is jugular drainage in 72% of healthy volunteers.26 In 22% related to the CSF loss from the cranial to the spinal com- the jugular drainage equals the nonjugular drainage, and partment, usually about 3 ml, which is due to the differ- in 6% the drainage pattern is nonjugular. These findings ential in compliance of the 2 compartments.54 In contrast, suggest that in the general population there are variations in patients harboring shunts without antisiphon devices, in the anatomy of cranial venous outflow.7,82,94 pressures range from -15 to -35 cm H2O when they are Human cerebral venous outflow depends on central upright.15,41,45 One method that allows us to quantify the venous pressure and posture.26,36,63 A marked increase in cerebral venous pressure component of ICP during CSF central venous pressure, such as any Valsalva maneuver, diversion is Davson’s steady-state formula,23 ICP = Pcv + completely reopens the internal jugular veins.26 In an ul- (If × Ro), where Pcv is cerebral venous pressure, If is CSF trasonography study of the postural dependency of venous formation rate (usually 0.3 ml/min), and Ro is CSF outflow outflow, it was shown that blood flow in the internal jugu- resistance. One can see that if CSF is withdrawn at the lar veins decreases from 700 ml/min in the supine position same rate as its production and because Ro approaches 0, to 70 ml/min at 90° elevation while flow in the vertebral ICP will reflect cerebral venous pressure. veins is increased from 40 to 210 ml/min.85 Total venous outflow declines from 740 to 280 ml/min from 0° to 90°, Pathophysiology of Cerebral Venous with the largest decrease at 15°. One important finding is that flow in the vertebral veins exceeds internal jugular Overdrainage vein flow at 45° of head elevation.85 The rigid spine seems The anatomy of the cranial venous outflow tracts is cru- to prevent epidural vein collapse, and negative epidural cial in the pathophysiology of cerebral venous overdrain- pressure may promote venous flow from the brain to the age. In the supine position the internal jugular veins are vertebral column.85 the main venous outflow pathways.28,82 During verticaliza- There is significant anatomical and functional conti- 2 Neurosurg Focus Volume 41 • September 2016 Unauthenticated | Downloaded 09/26/21 05:11 PM UTC Cerebral venous overdrainage associated with CSF diversion nuity between venous structures of the brain and spine. of the cranial cavity, that is, venous blood, was responsible Analogous to the CSF craniospinal axis, the venous out- for the drop in ICP referred to as “venous overdrainage.” flow network of the cranium and spine has been referred to as the “cerebrospinal venous system,” which is further Disease Entities Implicating Cerebral Venous enhanced by the lack of venous valves.82 During postural changes this anastomosis serves an important function in Overdrainage pressure homeostasis of the cerebral venous system.82 The A survey of the relevant literature revealed several suboccipital cavernous sinus, situated in the deep muscular categories of complications that might be explained by layers of the neck, serves as an important “relay station” cerebral venous overdrainage: 1) venous congestion or anastamosing with the 2 main divisions of the craniospi- engorgement in the spine causing mass effect, 2) suboc- nal venous system (cranial and spinal) in the suboccipital cipital venous congestion causing remote site intracranial region.3,20 It is connected to the jugular bulb and internal hemorrhage, 3) low pressure hydrocephalus, and 4) ven- jugular veins via the condylar veins and continues inferi- triculomegaly associated with craniectomy (Fig. 2). orly into