If the fluid in syrinx cavities is CSF and it has not reached the cavity directly from the fourth ventricle, it must flow across the cord tissue from the subarachnoid space. There has been much speculation about the possible route of such a fluid flow and the forces driving it.

In contrast to the proposal by Williams, Ball and Dayan suggested that a Chiari malformation would act to prevent spinal CSF from entering the cranial compartment during Valsalva manoeuvres (Fig. 6.2). They then speculated that the resulting increase in spinal CSF pressure could force CSF into perivascular spaces in the cord and that this fluid could coalesce to form a syrinx (Ball and Dayan 1972). Subarachnoid space obstruction from other causes such as post-traumatic arachnoiditis was said to produce a similar mechanism for fluid entry into the cord (Ball and Dayan 1972). The authors pointed to the pathological finding of enlarged perivascular spaces in syrinx cases as evidence for this theory.

Oldfield and colleagues proposed a similar mechanism, whereby the Chiari malformation imparts a piston-like effect on the spinal subarachnoid space, forcing fluid through either the perivascular spaces or interstitial spaces (Fig. 6.2) (Oldfield et al. 1994; Heiss et al. 1999). These authors provided cine-MRI and intra-operative ultrasound evidence of cerebellar tonsil movement in support of their theory, but had no direct evidence for fluid flow into the cord.

Support for a perivascular flow of fluid has arisen from the experimental work of Stoodley and colleagues, who used tracers of CSF bulk flow to demonstrate perivascular flow from the subarachnoid space to the central canal in normal animals (Stoodley et al. 1996, 1997), and from Klekamp et al., who showed oedema and enlarged perivascular spaces in a model of arachnoiditis (Klekamp et al. 2001). Further work showed that perivascular flow of CSF from the subarachnoid space occurs in models of canalicular and extracanalicular syringomyelia (Fig. 6.3) (Stoodley et al. 1999; Brodbelt et al. 2003b) and that flow is dependent on arterial pulsations (Stoodley et al. 1997).

A major problem with any proposed explanation for syrinx formation from a trans-parenchymal flow of CSF from the subarachnoid space is the simple physical fact that increasing pressure on the outside of the cord cannot create an expanding cyst within the cord. For a cavity to enlarge, the pressure within it must exceed the surrounding pressure, and this cannot occur with flow that is driven by an increase in pressure in the subarachnoid space. Several investigators have attempted to address this. Bilston and colleagues have examined the pulsatile properties of fluid flow in perivascular spaces and the subarachnoid space (Bilston et al. 2003, 2010). Using computational modelling, they demonstrated that the anatomical characteristics of the perivascular space could act as a ‘leaky’ one-way valve for pulsatile CSF flow. In addition, a timing mismatch between the arterial wave and CSF pressure wave arriving at the interface between the subarachnoid space and the perivascular space could act to increase flow (Fig. 6.4). They indicate this occurs when the CSF peak pressure occurs at a different time to the arterial pulse peak pressure, resulting in lower resistance to CSF inflow than outflow (Bilston et al. 2010). It was suggested that Chiari malformation and other obstructions in the subarachnoid space could act to create the timing mismatch.

An alternative explanation is that stenosis of the subarachnoid space could lead to a focal increase in pressure in the spinal cord with Valsalva manoeuvres, the so-called ‘elastic jump ’ (Carpenter et al. 2003). Although computational modelling has shown this to be a theoretical possibility, the magnitude of the effect appears to be too small to be significant (Elliott et al. 2009).

It appears likely that there is a continual flow of fluid into the spinal cord and also into syrinx cavities. Unless a syrinx is enlarging, the outflow must equal the inflow. The physiology of fluid outflow is not known, but one possible explanation for syrinx formation and enlargement is the obstruction of outflow. This concept was initiated by Ellertsson and Greitz, who measured syrinx and subarachnoid space pressures in patients, showing higher pressure in syrinx cavities, although this was not significant. They suggested an impairment of outflow, although did not speculate as to the mechanism of this (Ellertsson and Greitz 1970).

Aboulker suggested that the pressure on the spinal cord at the cervicomedullary junction prevents CSF draining rostrally along the central canal to the fourth ventricle (Aboulker 1979). Although such a rostral flow has been demonstrated in experimental animals, it is not known whether this occurs in humans (Milhorat et al. 1991). Theoretically, fluid could also drain through spinal cord parenchyma, and cord compression might compress the extracellular space or reduce permeability, thus restricting outflow.

Recently, Koyanagi and Houkin have suggested that an increase in spinal venous pressure might impair absorption of extracellular fluid, resulting in accumulation of fluid in the cord and syrinx formation (Koyanagi and Houkin 2010).

There is little clinical or experimental evidence to support or refute these theories. The physiology of fluid outflow from the spinal cord and syrinx cavities is a largely unexplored area that may be important in syringomyelia physiology and is deserving of more research attention.

Rather than fluid being forced into the cord by pressure changes in the subarachnoid space or physiological changes in perivascular flow, an alternative view is that pressure exerted on the cord surface causes rostral-caudal dissection of an existing cavity, leading to enlargement of the cavity. This concept began with the description by Williams of a ‘suck and slosh ’ mechanism for expansion of post-traumatic syrinx cavities. He suggested that increases in pressure in the subarachnoid space cause pressure on a cavity, which then dissects into the surrounding cord tissue, enlarging the potential space for the cavity, which then fills with extracellular fluid (Williams 1992). This mechanism has also been supported by the work of Oldfield and colleagues (Oldfield et al. 1994), who used intra-operative ultrasound to show that the cord and syrinx became compressed with each arterial pulsation and in synchrony with the descent of the cerebellar tonsils of a Chiari malformation. They suggested that this compression would cause extension of the syrinx cavity and that the fluid filling the cavity came from the subarachnoid space.

These theories rely on the presence of an initial cavity that can subsequently be enlarged by the putative dissection process. It is possible that this may apply to post-traumatic syringomyelia, where initial cavities form from haemorrhage and ischaemia. However, there is no evidence for a similar process in those cases associated with Chiari malformation. In addition, this process could at best explain the enlargement of a syrinx but not an increase in pressure relative to the subarachnoid space.

The available evidence does not support a fourth ventricular origin for syrinx fluid. There is good evidence that at least some syrinx fluid originates from the subarachnoid space and that the route of this fluid flow is via the perivascular spaces. However, theories that invoke increases in subarachnoid space pressure as the driving force are not sufficient to explain syrinx formation and enlargement. It is possible that complex relationships between CSF and arterial pulsations or the anatomical characteristics of the perivascular spaces explain the accumulation of fluid inside the cord. Pulsations exerted on the surface of the cord may contribute to cord tissue damage but seem insufficient to explain the development of high-pressure cavities. The possible role of perturbations in fluid outflow remains largely unexplored.

None of the hydrodynamic theories have adequately explained syrinx formation and enlargement. Alternative theories have been put forward to suggest that syrinx fluid is not of CSF origin and that hydrodynamic factors driving CSF flow are not responsible. These proposed mechanisms have been used to explain the development of cavities in association with intramedullary tumours , or have suggested that syrinx fluid is derived from interstitial fluid , or originates through abnormalities of the blood-spinal cord barrier or even cellular fluid transport mechanisms.