Cerebral DAVF is an acquired abnormal arterialto-venous
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1 Neurosurg Focus 32 (5):E10, 2012 Dural arteriovenous fistulas presenting with brainstem dysfunction: diagnosis and surgical treatment Charles Kulwin, M.D., Bradley N. Bohnstedt, M.D., John A. Scott, M.D., and Aaron Cohen-Gadol, M.D., M.Sc. Goodman Campbell Brain and Spine, Indiana University Department of Neurological Surgery, Indianapolis, Indiana A cerebral dural arteriovenous fistula (DAVF) is an acquired abnormal arterial-to-venous connection within the leaves of the intracranial dura with a wide range of clinical presentations and natural history. The Cognard classification correlates venous drainage patterns with neurological course, identifying 5 DAVF types with increasing rates of symptomatic presentation. A spinal DAVF occurs when a radicular artery makes a direct anomalous shunt with a radicular vein within the dural leaflets of the nerve root sleeve. A cervical DAVF is a rare entity, as most spinal DAVFs present as thoracolumbar lesions with myelopathy. In this paper the authors present 2 patients presenting initially with brainstem dysfunction rather than myelopathy secondary to craniocervical DAVF. The literature is then reviewed for similar rare aggressive DAVFs at the craniocervical junction presenting with brainstem symptomatology. ( Key Words arteriovenous fistula brainstem dysfunction surgical ligation diagnosis Cerebral DAVF is an acquired abnormal arterialto-venous connection within the leaves of the intracranial dura with a wide range of clinical presentations and natural history. 1 3,5 Although many classification systems have been proposed in an attempt to separate benign from aggressive (associated with a future risk of intracranial hemorrhage) fistulas, the most common ones are the Borden and the Cognard classification systems. Both systems have been validated in the literature. 4 The Cognard classification 3 correlates venous drainage patterns on angiography to neurological course, identifying 5 DAVF types with increasing rates of symptomatic presentation. Although Cognard Types I IV DAVF involve only dural sinus or cortical venous drainage, Type V fistulas are unique in harboring spinal perimedullary venous drainage. These Type V fistulas carry a risk of future neurological decline and are very rare; in large intracranial DAVF series, they typically represent < 5% of all DAVFs. 3,4 As classically described, a Type V DAVF presents with progressive myelopathy, leading to development of brainstem compromise later in the disease process; only rarely described are the symptoms and signs of initial brainstem dysfunction. A spinal DAVF occurs when a radicular artery makes Abbreviations used in this paper: ADC = apparent diffusion coefficient; DAVF = dural arteriovenous fistula; MMA = middle meningeal artery. a direct anomalous shunt with a radicular vein within the dural leaflets of the nerve root sleeve. A number of overlapping nomenclature systems have been proposed. A cervical DAVF is a rare entity; the majority of spinal DAVFs present as thoracolumbar lesions with myelopathy. Only a small number of cervical lesions have been described, and only 1 has been documented that presented with brainstem dysfunction. 13 In this paper we present 2 patients with brainstem dysfunction secondary to DAVF. One harbored a Cognard V DAVF and the other a cervical DAVF. We review the literature for similar rare aggressive DAVFs at the craniocervical junction presenting with brainstem symptomatology. Case Reports Case 1 This 44-year-old woman presented with acute onset of altered mental status, right hemiparesis, and limb dyscoordination. Subsequently, she became hypopneic when asleep and was transferred to a nursing home after undergoing a tracheostomy for central hypoventilation; the final diagnosis of her condition was brainstem stoke (Fig. 1). She subsequently developed episodes of abnormal limb movement, believed to be exacerbation of her brainstem ischemia based on neurological assessment. 1
2 C. Kulwin et al. Fig. 1. Case 1. Initial MRI demonstrating signs of brainstem venous congestion. A: Axial T2-weighted FLAIR image. B: Axial T1-weighted image with Gd enhancement. C: Sagittal T2-weighted FLAIR image. D: Axial ADC map. Retrospective evaluation of her initial workup, including CT angiography, revealed prominent skull-base/ high-cervical vasculature (Fig. 2). Formal angiography revealed a DAVF. The major arterial supply was the left MMA, with a minor arterial supply from a dural branch of the left vertebral artery (Fig. 3). The fistula connected to the left superior petrosal sinus with drainage via a perimesencephalic vein through the prepontine venous system and into the perimedullary venous plexus. Due to the persistent and progressive symptoms of her brainstem dysfunction, intervention was considered necessary. Open surgical disconnection of the fistula through a retromastoid craniotomy was performed. Two arterialized veins were found originating from the dura along the tentorial-petrous junction and were clip ligated; 1 traveled along the anterior brainstem and was ligated using a clip just anterior to the trigeminal nerve (Fig. 4.) She recovered well from surgery. Postoperatively, she Fig. 3. Case 1. Diagnostic digital subtraction angiography demonstrating the vascular anatomy of the DAVF. A: Left external carotid artery injection, midarterial phase, demonstrating arterial supply by the MMA. B: Left external carotid artery, venous phase, demonstrating drainage into perimedullary veins (asterisk). C: Left vertebral artery injection demonstrating contribution from the vertebral artery branch resulting in early venous filling (arrow). Fig. 2. Case 1. Initial sagittal (left) and axial (right) CT angiograms demonstrating prominent abnormal craniocervical vasculature. Arrows indicate dilated abnormal vessels. 2 progressively demonstrated improved right-sided motor function, albeit with residual paresis. Her chronic central hypoventilation was subsequently managed with phrenic nerve stimulation. Due to her stimulator, she could not undergo postoperative MRI evaluation.
3 Dural arteriovenous fistulas with brainstem dysfunction Fig. 4. Case 1. Intraoperative photographs. A: Open surgical disconnection of the fistula through a retromastoid craniotomy was accomplished, and 2 arterialized veins were found (asterisks) originating from the dura along the tentorial-petrous junction. B: One of these arterialized veins (asterisk) traveled along the anterior brainstem and was ligated using a clip just anterior to the trigeminal nerve. C: This ligation led to deflation and darker color of the arterialized anterior pontine vein (asterisk). Case 2 This 54-year-old woman presented with acute onset of left hemiparesis and diplopia. Intravenous thrombolytics led to minimal neurological improvement. Magnetic resonance imaging suggested ischemic infarction of the right inferior pons (Fig. 5). This infarction was presumed to be due to small vessel disease as no vertebrobasilar or cardiac source was identified. After discharge to rehabilitation, she suffered from another neurological decline with worsening of her left-side weakness and development of a new right-side weakness. New imaging studies revealed enlargement of her right pontine lesion and a new left pontine ischemic abnormality (Fig. 6). Cervical and cerebral angiography demonstrated a DAVF arising from the right vertebral artery (Fig. 7) originating from the right C-3 segmental branch of the artery, with medullary venous outflow draining in a cephalad direction along the cervical spinal cord and brainstem. A second stroke workup found no underlying cause for her progressive brainstem ischemia except for her cervical DAVF. The patient underwent a cervical laminectomy and DAVF disconnection. Intraoperative findings noted 3 fistulous vessels arising anteriorly adjacent to the C-2 nerve root, all of which were coagulated and cut (Fig. 8). She experienced progressive right-sided improvement in her strength after surgery. Follow-up 6-month MRI after surgery demonstrated no further areas of ischemia, decreased T2-signal change (indicating resolution of venous congestion), and small areas of pontine encephalomalacia (Fig. 9). Fig. 5. Case 2. Initial MRI demonstrating right pontine ischemia. sion-weighted image. C: Axial ADC map. Discussion Case reports of DAVFs presenting with primarily brainstem ischemia are very rare. Our literature search followed by a secondary review of the associated references in the primary sources revealed only 4 reported Cognard Type V DAVFs presenting as brainstem ischemia in the English literature, with a fifth case in the Japanese literature.6,8,9,11,12 Only 1 other cervical DAVF presenting with brainstem ischemia was found.13 These reported cases are summarized in Table 1. Dural arteriovenous fistulas adjacent to the craniocervical region most often present with progressive myelopathy related to spinal cord ischemia/venous hypertension.3,6 8,13 In this paper we report 2 such cases that atypically presented with brainstem ischemia. Although rare, the progressive natural history of these lesions and their resolution with intervention demonstrates the importance of detection in a timely fashion. Our first patient was initially diagnosed with a brainstem stroke, and no further workup was considered necessary. Our report emphasizes the need to further evaluate brainstem stroke of unknown origin through more comprehensive vascular studies, including cerebral angiograms. The primary mechanism responsible for brainstem dysfunction among the patients noted above is believed to be venous hypertension secondary to arterial pressure via the fistula. This mechanism has previously been suggested to cause potentially reversible venous congestion.10 In the first case, increased T2 signal changes within the brainstem without analogous diffusion restriction on A: Sagittal T2-weighted FLAIR sequence. B: Axial diffu- 3
4 C. Kulwin et al. Fig. 6. Case 2. Subsequent axial diffusion-weighted imaging (left) and ADC map (right) demonstrating progression of right pontine ischemia and new left pontine ischemia. diffusion-weighted imaging/adc mapping was consistent with previously described venous congestion that has been documented to resolve after fistulous disconnection.6 The typical ascending course is related to venous congestion. This congestion is observed initially in the anterior spinal vein, ascending via the anterior medullary vein to the anterior pontomesencephalic vein, worsened by vascular steal from normal spinal blood supply.8 However, due to the primarily external carotid arterial source, a steal phenomenon involving the spinal cord vessels was unlikely. This possibly explains the relative tolerance of the spinal cord to venous hypertension and resultant lack of myelopathy that usually dominates the initial presentation of Cognard Type V fistulas. In the second case, however, initial MRI was more suggestive of ischemic disease, with increased diffusionweighted signal and corresponding low ADC signal. In spite of this fact, a thorough embolic workup and empirical treatment with antiplatelet agents were unsuccessful. The patient s ischemic lesions and symptoms subse- Fig. 8. Case 2. Intraoperative photographs. A: Three fistulous vessels (arrow) arising anteriorly adjacent to the C-2 nerve root were found. B: Intraoperative temporary occlusion of the vessels revealed no change in the signals detected through the somatosensory and motor evoked potentials. C: All the fistulous connections were coagulated and cut. Fig. 7. Case 2. Diagnostic cervical digital subtraction angiograms demonstrating the vascular anatomy of the fistula, with anomalous early perimedullary venous filling (arrow), ascending toward the brainstem from a high cervical segmental branch of the right vertebral artery. Left: Right vertebral artery injection, midarterial phase. Right: Right vertebral artery injection, late-arterial phase, showing venous drainage of the fistula along the anterior spinal cord (arrow). 4 quently progressed. The presence of restricted diffusion combined with rostral vertebral blood supply suggests the possibility of a steal phenomenon, which could result in ischemia to tissue already at risk due to concomitant venous hypertension. The only prior case report of a cervical DAVF presenting with brainstem dysfunction did
5 Dural arteriovenous fistulas with brainstem dysfunction Fig. 9. Case 2. Follow-up 6-month axial MRI after surgery demonstrated no further areas of ischemia, decreased T2-signal change (indicating resolution of venous congestion), and small areas of pontine encephalomalacia. not include diffusion or ADC sequences, so the nature of the T2 hyperintensity cannot be similarly extrapolated. 13 However, given the pontine encephalomalacia noted on follow-up imaging, this ischemia does not appear to be similarly reversible as observed in brainstem venous hypertension. Our 2 cases demonstrate that although previous reports largely relied on endovascular embolization occlusion techniques, open surgical disconnection is feasible, safe, and efficacious for both cerebral and cervical lesions. Interestingly, in all cases with reported outcomes, the progressive neurological decline ceased, and prompt neurological improvement occurred (albeit mild in some instances) after fistulous interruption. Prior cases have demonstrated reversibility of the venous congestion-related dysfunction, emphasizing the importance of timely recognition and treatment, which mandates inclusion of a craniocervical DAVF in the differential diagnosis of new brainstem dysfunction. Finally, T2 hyperintensity without associated diffusion restriction may be more predictive of prompt recovery than findings of diffusion restriction, possibly due to an alternative mechanism of more reversible injury. Conclusions As shown by the 2 cases in this report, craniocervical DAVF should be considered in the differential diagnosis of ischemic brainstem dysfunction of unknown origin. Prompt diagnosis and treatment are important to provide the patient with the best chance at improvement. TABLE 1: Reported cases of craniocervical DAVF presenting with brainstem symptomatology* Neurological Outcome Venous Sinus Drainage Treatment Location of Dysfunction Arterial Source Type of DAVF Authors & Year Presenting Symptoms cerebral Li et al., 2004 vertigo, nausea & vomiting, paraparesis pontomedullary MMA, OA transverse coil embolization improved Oishi et al., 2005 disturbance of brainstem function medulla unknown superior petrosal coil embolization unknown Satoh et al., 2005 vertigo, nausea & vomiting, dysphagia, rt mo- medulla MMA, OA, APA, MHT, PMA transverse-sigmoid coil embolization improved tor & sensory changes Lagares et al., 2007 vertigo, quadriparesis, dysphagia, respiratory pontomedullary OA, PMA transverse surgical disconnection improved insufficiency Sugiura et al., 2009 nausea & vomiting, ataxia, nystagmus pontomedullary OA sigmoid coil embolization improved present study, Case 1 confusion, hemiparesis, ataxia pontomedullary MMA, PMA superior petrosal surgical disconnection improved cervical improved medulla C-6 segmental artery off VA spinal perimedullary vein coil embolization, surgical disconnection Terao et al., 2006 vertigo, orthostasis, urinary retention, paraparesis present study, Case 2 hemiparesis, diplopia pons C-3 segmental artery off VA spinal perimedullary vein surgical disconnection improved * APA = ascending pharyngeal artery; MHT = meningohypophyseal trunk; OA = occipital artery; PMA = posterior meningeal artery; VA = vertebral artery. Only available in Japanese literature. 5
6 C. Kulwin et al. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Cohen-Gadol, Kulwin. Acquisition of data: all authors. Analysis and interpretation of data: all authors. Drafting the article: all authors. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. References 1. Awad IA, Little JR, Akarawi WP, Ahl J: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72: , Brown RD Jr, Flemming KD, Meyer FB, Cloft HJ, Pollock BE, Link ML: Natural history, evaluation, and management of intracranial vascular malformations. Mayo Clin Proc 80: , Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, Casasco A, et al: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194: , Davies MA, TerBrugge K, Willinsky R, Coyne T, Saleh J, Wallace MC: The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg 85: , Dion J: Dural arteriovenous malformations: definition, classification and diagnostic imaging, in Awad IA, Barrow DL (eds): Dural Arteriovenous Malformations. Rolling Meadows, IL: American Association of Neurological Surgeons, 1993, pp Lagares A, Perez-Nuñez A, Alday R, Ramos A, Campollo J, Lobato RD: Dural arteriovenous fistula presenting as brainstem ischaemia. Acta Neurochir (Wien) 149: , Lasjaunias P, Chiu M, ter Brugge K, Tolia A, Hurth M, Bernstein M: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64: , Li J, Ezura M, Takahashi A, Yoshimoto T: Intracranial dural arteriovenous fistula with venous reflux to the brainstem and spinal cord mimicking brainstem infarction case report. Neurol Med Chir (Tokyo) 44:24 28, Oishi H, Horinaka N, Shmizu T, Ozaki Y, Arai H: [A case of intracranial dural arteriovenous fistula presenting with brainstem infarction.] No Shinkei Geka 33: , 2005 (Jpn) 10. Ricolfi F, Manelfe C, Meder JF, Arrué P, Decq P, Brugiéres P, et al: Intracranial dural arteriovenous fistulae with perimedullary venous drainage. Anatomical, clinical and therapeutic considerations. Neuroradiology 41: , Satoh M, Kuriyama M, Fujiwara T, Tokunaga K, Sugiu K: Brain stem ischemia from intracranial dural arteriovenous fistula: case report. Surg Neurol 64: , Sugiura Y, Nozaki T, Sato H, Sawashita K, Hiramatsu H, Nishizawa S: Sigmoid sinus dural arteriovenous fistula with spinal venous drainage manifesting as only brainstem-related neurological deficits without myelopathy: case report. Neurol Med Chir (Tokyo) 49:71 76, Terao T, Taniguchi M, Ide K, Shinozaki M, Takahashi H: Cervical dural arteriovenous fistula presenting with brainstem dysfunction: case report and review. Spine (Phila Pa 1976) 31:E722 E727, 2006 Manuscript submitted January 13, Accepted February 6, Please include this information when citing this paper: DOI: / FOCUS1217. Address correspondence to: Aaron A. Cohen-Gadol, M.D., M.Sc., Goodman Campbell Brain and Spine, Indiana University Department of Neurological Surgery, 1801 North Senate Boulevard #610, Indianapolis, Indiana acohenmd@gmail.com. 6
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