Dural arteriovenous fistula after craniotomy for pilocytic astrocytoma in a patient with protein S deficiency

Dural Arteriovenous Fistula After Craniotomy for Pilocytic Astrocytoma in a Patient with Protein S Deficiency Reza Yassari, M.D., Babak S. Jahromi, M.D., and R. Loch Macdonald, M.D., Ph.D. Section of Neurosurgery, Department of Surgery and Pritzker School of Medicine, University of Chicago, Chicago, Illinois

Yassari R, Jahromi BS, Macdonald RL. Dural arteriovenous fistula after craniotomy for pilocytic astrocytoma in a patient with protein S deficiency. Surg Neurol 2002;58;59 – 64. BACKGROUND

We report an unusual case, which may provide insight into the etiology and pathogenesis of dural arteriovenous malformation. CASE DESCRIPTION

A 24-year-old woman presented with hemorrhage into a pilocytic astrocytoma of the collicular plate. Angiography was normal and the tumor was surgically resected. She developed sigmoid sinus thrombosis and a transverse/ sigmoid sinus dural arteriovenous fistula 11 months after this and was found to have protein S deficiency. The fistula was not treated. Angiography 4 years later was unchanged. CONCLUSION

This report illustrates an acquired etiology of a dural arteriovenous fistula. To our knowledge this is the first reported case of postoperative sigmoid sinus thrombosis along with arteriovenous fistula in a patient with previously undetected protein S deficiency. © 2002 by Elsevier Science Inc. KEY WORDS

Intracranial arteriovenous malformation, venous thrombosis, pilocytic astrocytoma, protein S deficiency.

ural arteriovenous malformations of fistulas account for 10 to 15% of all intracranial vascular malformations [3,19,30]. The prevailing opinion about their pathogenesis in adults is that they are acquired secondary to cerebral venous thrombosis and the associated venous hypertension that results from the thrombosis. The most common sites of cerebral venous thrombosis are the transverse and sigmoid sinuses and the incidence of

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Address reprint requests to: Dr R. Loch Macdonald, Section of Neurosurgery, MC3026, University of Chicago Medical Center, 5841 South Maryland Avenue, Chicago, IL 60637 Received October 29, 2001; accepted February 5, 2002. © 2002 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010

involvement of each sinus is about equal [19]. Precipitating factors for cerebral venous thrombosis may be thought of as producing alterations in flow in the sinus or vein, abnormal blood coagulation, or damage to the sinus or vein itself. Cerebral venous thrombosis has been reported in association with intracranial surgery [29,35,40], intracranial tumors or infection [4,42], craniocerebral trauma [5], congenital or acquired hematologic abnormalities, pregnancy and the purpureum, systemic volume depletion, and systemic infection or malignancy [7]. We present an unusual clinical situation in which a patient who underwent craniotomy for tumor resection later developed sigmoid sinus thrombosis and a dural arteriovenous fistula, and was found to have a previously undetected, hereditary coagulopathy.

Case Report A 24-year-old woman developed sudden onset of severe headache during sexual activity. Neurological examination was normal. Cranial computed tomography (CT) scan showed acute hydrocephalus with a ventriculocranial ratio of 0.21. There was acute hemorrhage in the midbrain tectum with subarachnoid hemorrhage over the superior surface of the cerebellum. A four-vessel cerebral angiogram showed no arteriovenous malformation or aneurysm (Figure 1). There was lateral displacement of the medial divisions of both superior cerebellar arteries and the superior vermian arteries, and evidence of ventricular dilation. The external carotid arteries were not injected so the presence of a dural arteriovenous fistula fed by these arteries cannot be excluded, although the patient had no tinnitus before the ictus and venous drainage from the vertebral artery injections was through the left trans0090-3019/02/$–see front matter PII S0090-3019(02)00730-9

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Right vertebral artery angiogram, anteroposterior view of venous phase, showing predominant drainage into the left transverse and sigmoid sinuses without evidence of irregularity of the sinuses.

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verse and sigmoid sinus, suggesting that there was no high-pressure arterial inflow into these sinuses. Furthermore, the transverse and sigmoid sinuses and internal jugular veins were visualized bilaterally. Complete blood count, platelet count, bleeding time, prothrombin time, and partial thromboplastin time were normal. Cranial magnetic resonance imaging (MRI) 36 hours after onset of the headache showed a mass in the quadrigeminal plate with associated hydrocephalus (Figure 2). This was hypointense on T1- and hyperintense on T2-weighted images and showed areas of hyperintensity on T1weighted images in keeping with acute hemorrhage. There was a ring-enhancing area in the lesion. The sigmoid and transverse sinuses were patent and there was no abnormal vascularity or enhancement of the dura in the region where the dural fistula was later noted. She underwent midline, suboccipital craniotomy in the Concorde position and a tumor was resected from the collicular plate region. The dura was normal without evidence of dural arteriovenous fistula on the left side. No neurological deficit or abnormality of eye movements was detected postoperatively. Histologic examination identified the tumor as a pilocytic astrocytoma. An MRI 6 months later showed no enhancement (Figure 3). There were areas of hypointensity on T1- and hyperintensity on T2-weighted images around the lateral margins of the resection cavity that did not change on subsequent MRIs obtained up to 4 years later. Ventricular size remained unchanged. No signal abnormalities to suggest venous sinus thrombosis were visible on the pre- or postoperative MRI (Figure 3). The patient recovered uneventfully. The patient returned 11 months after the initial presentation complaining of a several-week history of pulsatile tinnitus in the right ear that seemed to

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start after a viral upper respiratory tract infection. Neurological examination was normal, no bruit was audible and an MRI showed, in addition to the intracranial changes noted above, bilateral mastoid air cell opacification compatible with sinusitis. Two months later, the pulsatile tinnitus had become louder and was audible in both ears. Examination showed that the left occipital artery pulse was now more prominent than the right and there was a bruit over the right transverse sinus. An angiogram was obtained which demonstrated a dural arteriovenous fistula with arterial supply from branches of the left occipital, posterior auricular, and middle meningeal arteries (Figure 4). The fistula entered the left transverse sinus and drained across the torcula to the right side. The left sigmoid sinus was occluded. There was no retrograde leptomeningeal venous drainage. MRI suggested thrombosis in the sigmoid sinus and internal jugular vein. Ophthalmologic examination revealed leakage of the left optic disc on fluorescein angiogram indicating early papilledema although there was normal visual acuity and intraocular pressure. Hematologic values showed normal levels of protein C and antithrombin III. There was no factor 5 Leiden or antiphospholipid antibodies. Protein S was decreased at 62% (normal: 69%–169%) and was confirmed on a second screen at 56%. There was no family history of venous thromboembolism or fetal wastage. The patient was not on any medications. Treatment for the fistula was not recommended in the absence of retrograde leptomeningeal venous drainage or overly bothersome tinnitus. It was recommended that short-term anticoagulation be considered during pregnancy or situations predisposing to venous thromboembolism such as some surgical procedures and prolonged airplane travel. An MRI and cerebral angiogram 4 years later were unchanged.

DISCUSSION We report the unusual association of hemorrhage into a pilocytic astrocytoma, venous sinus thrombosis, dural arteriovenous fistula, and protein S deficiency. Development of dural arteriovenous fistulas in adults often is associated with thrombosis or occlusion of the involved sinus [15,16,19,41,42]. It has been suggested that dural arteriovenous fistulas are acquired lesions that develop from enlargement and proliferation of small, arteriovenous connections that are present normally in the walls of the major venous sinuses [14,31]. The stimulus for development is permanent or transient sinus thrombosis. There are cases reported, however, in

DAVF and Protein S Deficiency

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Axial T1-weighted magnetic resonance images after administration of gadolinium show an irregular, ring-enhancing mass in the collicular plate (A) associated with hydrocephalus. The transverse (B) and sigmoid sinuses (C, D) are patent and there is no evidence of abnormal vascularity in the dura on the left side.

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which there is no evidence of pre-existing thrombosis, suggesting that in some cases the dural fistula causes the thrombosis because of high-flowinduced vasculopathy [5,25]. It is possible that the inciting thrombosis resolves in some cases or that thrombosis is secondary to abnormally high flow through the sinus and is a result, rather than a cause, of the fistula. In addition, the occurrence of dural arteriovenous fistulas in neonates and children points toward a congenital origin, at least in this group or a subgroup of these patients [1,27,28]. A possible sequence of events in the pathogenesis of acquired DAVF could involve intrinsic arteriovenous communications that exist in the dura mater. An increase in venous pressure after sinus thrombosis could open these channels because of the increased arterial pressure necessary to maintain antegrade flow [14,18]. These changes result in an arterialization of the venous portion and exacerbation of the unfavorable hemodynamic condition, promoting the creation of arteriovenous fistulas. The hemodynamic changes, if extensive, can result

in reduced cerebral perfusion and venous ischemia [6,22]. The ensuing tissue hypoxia will stimulate angiogenesis and perivascular neovascularization. Abnormal angiogenic activity could then contribute to the formation of the fistula [24,37]. The formation of a dural arteriovenous fistula can further increase venous pressure, thus creating a vicious circle. Cerebral venous thrombosis may be precipitated by infectious and non-infectious causes [2,7]. In addition to well-known predisposing conditions, coagulopathies such as protein C deficiency, antithrombin III deficiency, protein S deficiency, and activated protein C resistance, usually on the basis of a mutation of factor V called factor V Leiden are now recognized to underlie many cases of both cerebral and systemic venous thrombosis and often are found in combination with other etiologies [8,9, 11,12,17,26,38,43]. The patient described here had protein S deficiency. Transient or permanent protein S deficiency and cerebral venous thrombosis has been reported in association with systemic lupus erythematosis [23], acquired immunodefi-

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Axial T1-weighted magnetic resonance image after administration of gadolinium obtained 4 years after the initial presentation show a cavity at the site of the prior tumor with surrounding hypointensity. There is hydrocephalus, as suggested by the size of the temporal horns and suprachiasmatic portion of the third ventricle visible on this image, which is unchanged from previous studies.

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ciency syndrome [21], ulcerative colitis [38], pregnancy [10,13], and the purpureum [9,12]. The activated protein C-protein S complex inhibits clotting by proteolytically cleaving factors Va and VIIIa [36]. Protein S exists as an active free form that is able to act as a co-factor for protein C and an inactive form that is bound to C4b-binding protein [39]. An increase in the C4b-binding protein level results in an elevation of the bound, inactive form of protein S, and as a consequence, a decrease of the free, active form. This may create a prothrombogenic state. C4b-binding protein is an acute phase protein and is elevated in inflammatory responses and acute infections. Major surgery evokes an acute-phase response and transient immunosuppression with normal function usually restored after a few days [33]; however, in a subgroup of patients homeostasis may be lost and development of the systemic inflammatory response syndrome ensues [32]. Mild forms of the systemic inflammatory response syndrome are frequent in medical and surgical patients and may correspond to the

Left common carotid artery angiogram, anteroposterior (A) and lateral (B) views of arterial phase, showing a dural arteriovenous fistula supplied by branches of the external carotid artery and draining into the transverse and sigmoid sinuses. Outflow is predominately across the midline to the right side. A right vertebral artery angiogram, anteroposterior view of venous phase (C), now shows predominant drainage into the right transverse and sigmoid sinuses.

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common postoperative febrile state. This patient had an unrecognized, underlying mild form of protein S deficiency but the levels were presumably enough to maintain normal homeostasis. A transient increase in acute phase proteins associated with surgery or upper respiratory tract infection could have promoted a pro-thrombogenic state, resulting in sinus thrombosis and subsequent formation of a dural arteriovenous fistula. The thrombosis was not observed on postoperative MRIs until the tinnitus had developed, suggesting that surgery was not the inciting event. Witt and colleagues described a 1-year-old, previously healthy child who presented with generalized tonic-clonic seizures and was diagnosed with massive thrombosis of the cerebral venous system and coexisting dural arteriovenous malformation [41]. The child had had symptoms of an upper respiratory tract infection for days before developing seizures. The development of dural arteriovenous fistulas weeks to months after an upper respiratory infection was noted in our patient and has been previously described [37]. Mechanisms might include transient alterations in coagulation parameters or extension of inflammation into the mastoid or other air sinuses, potentially promoting venous thrombosis. Dural arteriovenous fistulas have been reported after surgery for posterior circulation aneurysms, meningiomas, brain abscess, trigeminal rhizotomy, craniopharyngioma, microvascular decompression for hemifacial spasm, superficial temporal artery-tomiddle cerebral artery bypass, and trigeminal schwannoma [20,29,35,40]. The fistula usually was detected months to years after the initial surgery and in some cases was remote from the surgery but in others, involved a sinus that might have been exposed at surgery. Most reports predated the recognition of the above-noted coagulopathies. Sakaki et al reported 5 patients who developed dural arteriovenous fistulas of the transverse-sigmoid sinus junction 2 to 6 years after surgical occlusion of the sigmoid sinus performed during resection of tumors [34]. The authors suggested that increased intrasinus pressure or thrombosis led to the development of the fistula. Multiple factors may be invoked to explain the development of a fistula. Patients would normally not develop one after surgery near a sinus but the risk might be increased by underlying coagulopathy, transient or permanent sinus thrombosis induced by surgical retraction or compression by tumor, or angiogenesis induced by surgery or a neoplasm. Underlying coagulopathy might lead to sinus thrombosis remote from the site of surgery. The role of some process that increases

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COMMENTARY

The development of acquired dural arteriovenous fistula following trauma or craniotomy has been widely reported. However, the mechanisms of lesion pathogenesis remain speculative. In this nice report, the authors demonstrate a hypercoagulable state and dural sinus thrombosis, both of which had been implicated in the pathogenesis of such lesions. It remains to be elucidated in future studies which of these factors, and other contributing risk factors, are necessary and sufficient for the genesis and progression of dural AV fistulae. Issam A. Awad, M.D. Department of Neurosurgery University of Colorado Denver, Colorado