5.2.4

Venous Hypertension

The concept of venous hypertension, being another key factor in the etiology of DAVFs, is encouraged by results of animal experiments conducted by Terada et al. (1994), who demonstrated that increased venous pressure can cause newly acquired AVFs, even in absence of thrombosis. It can be suspected that a similar mechanism may also play a role in humans (Phatouros et al. 2000). Kusuka et al. (2001) recently reported the development of a DCSF remotely from a previously thrombosed lateral sinus that developed another DAVF, emphasizing the role of venous hypertension. The authors conclude that the thrombosis caused venous hypertension not only within the superior sagittal and right transverse/sigmoid sinus, but also in the CS, causing here micro AV shunts within the dura mater to open and eventually to trigger the DCSFs. This is an interesting interpretation, but raises some questions. First, there was no direct evidence that the CS was in fact exposed to an increased venous pressure. Second, one would probably expect another fistula to develop in the neighborhood of the thrombosed lateral sinus where most likely the venous pressure was elevated. The hemodynamic effects associated with dural arteriovenous shunts in the sigmoid/transverse sinus area may be more complex than assumed and our knowledge on this subject is still limited.

The role of venous hypertension as etiological factor is reassured by another observation. A possible causal relationship between hypertension and arteriovenous shunts at the CS has already been assumed by Potter (1954) as well as by Echols and Jackson (1959), who suggested that creating hypotension might be beneficial for causing spontaneous thrombosis of a CCF. There are anecdotal reports that symptoms and signs caused by a CSF have disappeared after air travel (Debrun et al. 1988a; Kupersmith 1988). I have seen one patient who noticed his bruit, caused the first time by a sigmoid DAVF immediately after landing in an airplane. Another more recent patient with a DCSF reported a drastic increase in eye swelling and redness following a 3-h flight. Changes of atmospheric pressure seem to interfere with pressure in the cerebral venous system. They may have a bidirectional effect on the arteriovenous shunt flow, causing either an increase, or a decrease with spontaneous occlusion.

Ornauqe et al. (2003) have successfully applied this concept to treat patients with DAVFs and DCSFs using controlled hypotension (see also Sect. 9.3).

Lawton et al. (1997) were able to demonstrate a causal relationship between venous hypertension and angiogenic activity and DAVF formation. The authors suggested that venous hypertension is induced by a venous outflow obstruction due to a thrombus and may initiate the pathogenesis of a DAVF. Venous hypertension can cause ischemia and tissue hypoxia that may stimulate angiogenesis. This “aberrant” angiogenic activity of dural vessels could lead to arteriovenous shunting and formation of a DAVF. The subsequent arterialization will increase venous pressure and outflow obstruction and thereby create the vicious cycle mentioned above that may enlarge the AV shunt and aggravate a DAVF into a progressive lesion.

5.2.5 Trauma

Trauma, although reported in some anecdotal cases (Newton and Hoyt 1970), is probably less likely a cause of a DCSF (Tomsick 1997b). Sattler (1920) had doubts that minor trauma can indeed cause a pulsating exophthalmos and if so only if the vessel is “diseased already or in case of pregnancy”

(author’s translation). Tomsick (1997b) observed two patients with a spontaneous fistula after blunt head trauma, and one patient with a Type D fistula following rhizotomy. He emphasized the development of DCSFs following severe head trauma makes it difficult to define the exact etiology. The early series of Halbach et al. (1987) contained 1 patient while later, the same group reported on 234 traumatic carotid and vertebral artery lesions in which they observed 7 indirect fistulas. Berenstein et al. (1986) reported on 11 patients with DCSFs of which 1 was a traumatic fistula supplied by the MMA. Jacobson et al. (1996) described in detail two cases in which a ruptured AMA solely supplied a CSF.

True traumatic indirect fistulas represent possibly a specific entity of DCSFs since their angioarchitecture with a “single artery to single vein or sinus” pattern is distinctly different from the usual Type D fistula with a complex network of numerous feeders emptying into the CS. This typical angioarchitecture, on the other hand, can hardly be explained by trauma. Revascularization of a

thrombus (or more than one) in the CS with subsequent neovascularization and opening of multiple micro AV-shunts will most likely lead to a network of feeding vessels. Trauma and rupture will most certainly affect only one (or a few) of them, but will not create a network of vessels. A case of traumatic DCSF following craniectomy has been reported (Watanabe et al. 1984). Fields et al. (2000) described a 46-year-old patient who after sustaining a gunshot wound to his face developed a CSF supplied by dural ICA branches that completely disappeared 11 days after diagnostic angiography. Some iatrogenic CS fistulas may appear as single arteryCS shunts.

Aminoff (1973) considered the close anatomical relationship between dural arteries and veins a predisposition for the development of an AVF following head trauma. Moreover, the absence of trauma in the history would not exclude the possibility of minor head traumas causing an AVF in particular in children and young adults as a cause of DAVF.

Otherwise, many cases of DAVFs have no history of trauma and, even if they do, then there is usually an interval of several weeks or months before symptoms of an AV shunt appear. Thus, direct trauma seems unlikely to be a major cause for the development of DCSFs (Chaudhary et al. 1982). Tomsick (1997b) gave an overview that revealed approximately 3% of DCSFs are related to trauma. He observed an asymptomatic DCSF during diagnostic angiography for other indications, including one CCF on the contralateral side and concludes that major head trauma can cause DCSF. None of the patients with DAVFs or DCSFs in my own material could clearly be related to a relevant trauma. Despite justified skepticism on the role of trauma in the etiology of DAVFs and lack of sufficient proof, it should be considered that minimal trauma might be very difficult to evaluate as many patients will not recall minor events that could have resulted in the formation of an abnormal AV shunt.

Iatrogenic vessel injury during endovascular procedures may lead to AV shunts involving the CS and can be caused by transsphenoidal surgery of pituitary adenomas (Taptas 1982; Bavinzski et al. 1997). I have seen three iatrogenic direct CCFs in my practice, two patients after hypophysectomy and one patient who underwent septoplasty and presented with a high-flow CCF (Fig. 5.3). Catheterization of cavernous dural ICA branches for embolization of meningeomas may cause rupture and lead to an “in-

direct” CSF as well (Barr et al. 1995). Figure 5.4 illustrates such a case in which microcatheter manipulation into the marginal tentorial artery resulted in extravasation that fortunately resolved without clinical consequences.

5.2.6 Embolization

The de novo development of a DAVF in a sigmoid or transverse sinus in association with embolization of a DCSF has been reported several times and is explained by transvenous catheter manipulations with subsequent injury or by venous turbulence initiating thrombus and recanalization as a trigger (Nakagawa et al. 1992; Yamashita et al. 1993; Makiuchi et al. 1998; Kubota et al. 1999; Kawiguchi et al. 1999). Gupta et al. (2005) recently reported a case where 4 months after transarterial embolization of a DCSF a new AV shunt at the ipsilateral sigmoid sinus developed. Strangely enough, the opposite order of events, namely development of a dural CSF following embolization of a DAVF in other location, has to my knowledge not been reported.

5.2.7 Congenital

Although Lie (1968) proposed a congenital origin in some of the spontaneous CSFs, this etiology remains speculative. DAVFs in general, and DCSFs in particular are rare in childhood, and if they occur represent probably a separate entity (Biglan et al. 1981; Yamamoto et al. 1995). Biglan et al. (1981) observed a 7-week-old infant with a non-traumatic fistula between the external carotid artery and the cavernous sinus. Konishi et al. (1990) reported a case of a 2-month-old boy with a congenital fistula of the dural carotid-cavernous sinus. Skolnick and McDonnell (2000) recently reported on a 9-year- old boy who presented with proptosis, conjunctival congestion and decreased vision caused by spontaneous “dural cavernous sinus fistula”. Among other reasons, the fact that the cavernous sinus is not fully developed at birth and only partially participates in the cerebral venous drainage may explain why a typical dural CSF, as encountered in the adult population, is unlikely to occur in the pediatric age group.

5.2.8

Other Potential Factors

Recently, the role of basic fibroblast growth factor (bFGF) and vascular endothelial growth factor (VEGF) has been studied (Terada et al. 1996; Shin et al. 2003). bFGF, considered a powerful

angiogenic growth stimulator associated with the endothelial cell, was found with strong immunoreactivity in sinuses of patients with DAVFs (Malek et al. 2000). Uranishi et al. (1999) examined histologically dural AVFs that were surgically resected in nine patients and found that the thick wall of the dural sinus stained strongly

for bFGF, mainly in the subendothelial layer and media. VEGF was expressed in the endothelium of the sinus in all nine cases indicating that angiogenetic growth factors may play a role in the pathogenesis of DAVFs. This angiogenetic process could be associated with loss of venular surface properties and contribute to venous thrombosis (Sarma and ter Brugge 2003).

Lawton et al. (1997) were able to prove that angiogenic activity measured by the rabbit cornea assay was significantly greater in animals with venous hypertension, suggesting that the venous hypertension and sinus thrombosis may alter the balance

of proangiogenic and antiangiogenic substances (Folkman 1995).

5.2.9 Various

The higher incidence of DCSFs in women during menopause and in men over 50 years indicates a potential role of vessel wall weakening over time due to arteriosclerotic changes. Arterial hypertension and diabetes are considered predisposing factors as well, but correlative data are lacking so far.