Accepted Manuscript Recurring thalamic symptoms due to intracranial dural arteriovenous fistula: a report of an unusual case and its treatment outcome S. Vinayagamani, MD , DNB, Santhosh Kumar Kannath, MD, PDCC, Jayadevan Enakshy Rajan, MD , DNB , DM PII: S1878-8750(18)31403-7 DOI: 10.1016/j.wneu.2018.06.187 Reference: WNEU 8500 To appear in: World Neurosurgery Received Date: 29 March 2018 Revised Date: 21 June 2018 Accepted Date: 22 June 2018 Please cite this article as: Vinayagamani S, Kannath SK, Rajan JE, Recurring thalamic symptoms due to intracranial dural arteriovenous fistula: a report of an unusual case and its treatment outcome, World Neurosurgery (2018), doi: 10.1016/j.wneu.2018.06.187. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. ACCEPTED MANUSCRIPT TITLE PAGE Type of manuscript : Case report RI PT The title of the article: Recurring thalamic symptoms due to intracranial dural arteriovenous fistula: a report of an unusual case and its treatment outcome Running title or short title: Recurring thalamic symptoms due to intracranial dural arteriovenous fistula. AUTHORS M AN U SC 1) S Vinayagamani MD , DNB Senior Resident Department of Imaging Sciences and Interventional Radiology Sree Chitra Institute for Medical Sciences and Technology Trivandrum – 695011 , Kerala , India 2) Santhosh Kumar Kannath MD , PDCC Associate professor Neurointervention center Department of Imaging Sciences and Interventional Radiology Sree Chitra Institute for Medical Sciences and Technology Trivandrum – 695011 , Kerala , India EP TE D 3) Jayadevan Enakshy Rajan MD , DNB , DM Additional Professor Neurointervention center Department of Imaging Sciences and Interventional Radiology Sree Chitra Institute for Medical Sciences and Technology Trivandrum – 695011 , Kerala , India . AC C CORRESPONDENCE : Santhosh Kumar Kannath, Associate Professor, Neurointervention center , Department of Imaging Sciences and Interventional Radiology, Sree Chitra Institute for Medical Sciences and Technology Trivandrum – 695011 , Kerala , India. Ph No.- +91-471-2524117 Email: drsanthoshkannath@gmail.com The total number of pages-12 Total number of photographs- 4 ACCEPTED MANUSCRIPT Word counts for the abstract/summary-248 Word counts for the text-1358 AC C EP TE D M AN U • Source(s) of support in the form of grants, equipment, drugs, or all of these- None Acknowledgement- None If the manuscript was presented as part at a meeting, the organization, place, and exact date on which it was read- No Conflicts of interest- None SC • • • RI PT Key words: dural arteriovenous fistula , thalamic symptoms , venous aneurysm embolization. Vinayagamani ACCEPTED MANUSCRIPT RECURRING THALAMIC SYMPTOMS DUE TO INTRACRANIAL DURAL ARTERIOVENOUS FISTULA: A REPORT OF AN UNUSUAL CASE AND ITS TREATMENT OUTCOME RI PT SUMMARY: Background: Initial clinical presentation of DAVF with predominantly thalamic symptoms is rare and previously unreported. SC Case description: A young child presenting with complaints of tinnitus and mild right hemiparesis was evaluated with an initial MRI, which M AN U revealed a Borden type 2 DAVF in the right transverse sinus with retrograde venous drainage and cortical venous reflux. Flow related small aneurysms were also noted in the left basal vein of Rosenthal (BVR). Two days later, his motor power deteriorated and he developed right TE D hemisensory loss and severe thalamic pain. Aphasia was atypical and mimicked trans-cortical type. Repeat imaging revealed expanding EP thrombosed aneurysm of BVR with mass effect and edema on thalamocapsular region. Initial antiedema measures reversed the neurological AC C deficits, however it recurred, necessitating an urgent endovascular intervention. Angiogram revealed an extensive high flow DAVF in the right transverse-sigmoid sinus and torcula with preferential retrograde venous drainage into deep veins and left BVR. He underwent staged embolization of DAVF, resulting in significant obliteration of shunt. Neurological deficits improved in the postoperative period and patient remained clinically asymptomatic at 6 months of follow up. 1 Vinayagamani ACCEPTED MANUSCRIPT Conclusion: DAVF presenting with recurrent predominantly thalamic symptoms is rare. Atypical trans-cortical aphasia rather than fluent aphasia is an unusual clinical manifestation of thalamic pathology and could result RI PT from the involvement of specific thalamic nuclei. Preferential high flow into BVR in presence of venous anomalies could potentially induce architectural weakness of venous wall and precipitate aneurysm formation. SC Embolization of the DAVF can potentially reverse this unusual BACKGROUND: M AN U neurological condition. Intracranial dural arteriovenous fistulae (DAVF) are rare type of acquired TE D pathological shunting between dural arterial branches and dural venous sinus, meningeal or cortical veins. The most common locations are EP transverse sinus, sigmoid sinus, torcula and cavernous sinus1. DAVF may present with innocuous symptoms such as tinnitus, headache or with AC C aggressive manifestations such as intracranial bleed or non-hemorrhagic neurological deficits. Other uncommon initial manifestations include dementia, parkinsonism, aphasia, myoclonus, alexia or myelopathy2,3. Initial clinical presentation of DAVF with predominantly thalamic symptoms is rare and previously unreported. We report a rare case of paediatric DAVF presenting with clinical features of recurrent transient subcortical aphasia, fluctuating hemiplegia and hemisensory pain, all 2 Vinayagamani ACCEPTED MANUSCRIPT attributed to thalamic etiology. The clinical and radiological correlation of this unusual neurological presentation and its outcome following RI PT endovascular treatment is discussed. SC CASE REPORT: A 11 year old male child presented with complaints of tinnitus, mild M AN U weakness of right upper and lower limb and right eye proptosis for past 2 months. On examination, patient had mild right hemiparesis with pyramidal signs and right upper motor neuron type of facial palsy. Rest of the neurological examination including higher cognitive functions were TE D normal. There was mild proptosis of right eye and fundus examination revealed bilateral hyperemic optic discs. His baseline hematological and EP biochemical investigations were normal. Initial MRI and CT examination revealed right transverse sinus– sigmoid sinus (TS-SS) DAVF with Small draining venous AC C enlarged and dilated cortical venous system. aneurysm measuring 1.8x1.6 cm arising from left basal vein of Rosenthal (BVR) was also seen, indenting the left thalamocapsular region. (Fig 1A,B). Patient was planned for cerebral angiogram and definitive treatment, however two days later, he developed hemiplegia, severe pain, numbness and hemisensory loss confined to the right half of the body and face. He also developed aphasia characterized by dysfluency, low auditory 3 Vinayagamani ACCEPTED MANUSCRIPT comprehension, loss of naming and writing with fairly preserved repetition. A possibility of thalamic stroke or hemorrhage was considered and urgent imaging was obtained. CT and MRI (Fig 1E&F) revealed an expanding RI PT venous aneurysm of BVR, with peripheral thrombosis and perilesional edema involving the posterior part of the thalamus (pulvinar region). Child was initially managed conservatively with antiedema measures. Few hours SC later, patient showed marked improvement in motor power with resolution of thalamic pain and aphasia, which again worsened one day later. Digital M AN U subtraction angiogram (DSA) under general anaesthesia revealed an extensive DAVF involving right TS-SS and torcula (Cognard 2a+2b, Borden 2) with feeders from bilateral posterior meningeal arteries, parietal, petrosquamosal and basal tentorial branches of middle meningeal artery TE D (MMA) and tentorial branches of cavernous internal carotid artery (ICA) (Fig2A,B). Venous drainage was noted into the right transverse sinus, with predominant retrograde reflux into superior sagittal sinus and straight sinus. EP (Fig2A-C). Due to the occlusion of right sigmoid sinus and tight stenosis of AC C left jugular bulb, there was preferential reflux into the deep veins and left basal vein of Rosenthal, which demonstrated aneurysmal outpouching in its second and third segments. Compared to the initial imaging a significant increase in size (3.4X2.5cm) was evident.(Fig 2C,D). Following angiogram, a 6Fr Envoy guide catheter (Codman, Wokingham, UK) was placed in the proximal internal maxillary artery and the petrosquamosal branch of left MMA was accessed using an Apollo 3 cm detachable tip 4 Vinayagamani ACCEPTED MANUSCRIPT microcatheter (Covidien/Medtronic, Irvine, California, United States) and Mirage microguidewire (Covidien/Medtronic, Irvine, California, United States). A total of 9.6 ml of onyx was injected under roadmap guidance, RI PT achieving partial reduction in the size of the fistula (Fig 2E). In the postoperative period he demonstrated gradual recovery of residual neurological deficits and the child was discharged on 5th postoperative day. SC Patient made complete neurological recovery at 3 months clinical follow up and MRI evaluation demonstrated resolution of mass effect in the thalamus M AN U and reduction in the size of venous aneurysm (Fig 2F). Subsequently, patient underwent a second sitting embolization and significant obliteration DISCUSSION: TE D of the residual DAVF was achieved (3A-C). Clinical presentations of DAVF depend on angiomorphological features such as the dural venous outflow pattern, cortical venous reflux and the site EP of the fistula1. Benign cranial DAVF may be asymptomatic (2.6%) or more AC C commonly presents with ocular symptoms (39.3%) and chronic headache(32.5%), with the incidence of hemorrhagic focal neurologic deficit being very low (1.5%)1,2. Aggressive DAVF presents with intracranial hemorrhage (62%) or non-hemorrhagic neurological deficits like seizure (14%), visual symptoms (7%) and bruit (3%)1-3. Rarely DAVF can also present with uncommon clinical symptoms such as dementia or parkinsonism4,5. Intracranial DAVFs rarely drains into spinal 5 Vinayagamani ACCEPTED MANUSCRIPT perimedullary vein, producing venous congestion and ischemic myelopathy6. To the best of our knowledge, only four cases of aphasia due to DAVFs has RI PT been reported. Katz et al7 reported a case of transient global aphasia caused by a giant sagittal sinus dural AV fistula due to ipsilateral hemispheric venous congestion. Chou et al8 and Nourbakhsh et al9 also SC reported a case of sensory cortical aphasia due to temporal lobe edema in left transverse sinus and sigmoid sinus DAVF. Togawaet al10 reported a M AN U case of global aphasia without hemiparesis caused by DAVF of left isolated transverse sinus with leptomeningeal venous drainage. The exact mechanism of cortical aphasia was attributed to the laminar necrosis of left temporal lobe (dominant) due to long standing venous congestion related TE D ischemia. All these four cases were presented with cortical aphasia (global or sensory) due to temporal lobe dysfunction as a result of left TS-SS EP DAVF. Holekamp et al5 also reported venous congestion induced thalamic manifestations like dementia and aphasia, where the exact type and cause AC C of aphasia was not discussed. Our case is unique due to fact that the patient had recurrent thalamic symptoms, which was induced by the increasing mass effect on thalamus by flow related venous aneurysm. However, the type of aphasia observed in our patient was atypical of thalamic or striatocapsular etiology and it mimicked trans-cortical type of aphasia. The evolution of the clinical symptoms in our case could be explained by the anatomical variations of venous system and hemodynamics of DAVF. Due 6 Vinayagamani ACCEPTED MANUSCRIPT to the steno-occlusive lesions of bilateral jugular bulbs, there was significant retrograde shunting of fistula flow into the deep veins, which was preferentially redirected to the left BVR, as the right BVR was RI PT hypoplastic in its third segment. Increased hemodynamic stress due to the arterialised flow might have lead to the remodelling and weakening of venous wall and eventually resulted in the aneurysm formation11,12. Indeed, SC pathological studies in DAVFs with chronic venous hypertension have confirmed the development of venous aneurysms in the arterialized veins11. M AN U The dilated and tortuous BVR might manifest tight curvatures along its course, where flow impingement and resulting shear stress will be high. These sites might show high predilection for aneurysm formation and indeed in our case (figure 4A,B), we observed these aneurysms at the EP Rosenthal11,12. TE D junction of acute bends in the second and third segments of basal vein of Episodic increase in mass effect and edema by expanding thrombosed AC C venous aneurysm could explain the recurrent thalamic symptoms observed in our patient. The aphasia caused by the involvement of thalamus or striatocapsular region are categorized as subcortical aphasias, which can be fluent type with impaired comprehension or a dysfluent type with preserved comprehension respectively13. In our case, aphasia is characterized by speech dysfluency, low comprehension with loss of reading, naming and fairly preserved repetition, mimicking a transcortical 7 Vinayagamani ACCEPTED MANUSCRIPT variety13,14. Radanovic et al reported that thalamic aphasia with dysfluency and low comprehension could be possible with involvement of specific areas like left ventrolateral nucleus , pulvinar and paramedian nuclei14-16. RI PT Indeed in our patient, the edema and the mass effect by the venous aneurysm involved left pulvinar and paramedian nuclei, which could potentially explain this unusual clinical manifestation. To the best of our SC knowledge, this is the first report that describes recurrent and transient thalamic symptoms as an initial clinical manifestation of M AN U DAVF. intracranial CONCLUSION We report a rare case of intracranial dural arteriovenous fistula (DAVF) TE D presenting with fluctuating thalamic symptoms secondary to mass effect on thalamus by an expanding venous aneurysm of basal vein of Rosenthal. EP Preferential high flow into BVR could potentially induce architectural weakness of venous wall, especially at tight curvatures and precipitate AC C aneurysm formation. Embolization of the DAVF can potentially reverse this unusual neurological condition. REFERENCES 8 Vinayagamani ACCEPTED MANUSCRIPT 1. Gandhi D, Chen J, Pearl M, Huang J, Gemmete JJ, Kathuria S. Intracranial dural arteriovenous fistulas: classification, imaging findings, and treatment. AJNR Am J Neuroradiol. 2012;33(6):1007-1013. Miller TR, Gandhi D. Intracranial Dural Arteriovenous Fistulae: Clinical RI PT 2. Presentation and Management Strategies. Stroke. 2015;46(7):2017-2025. 3. Chaichana KL, Coon AL, Tamargo RJ, Huang J. Dural arteriovenous fistulas: Gopinath M, Nagesh C, Santhosh K, Jayadevan ER. Dementia and Parkinsonism-a Rare Presentation of Intracranial 2017;12(2):125-129. 5. Dural Arteriovenous Fistulae. Neurointervention. M AN U 4. SC epidemiology and clinical presentation. Neurosurg Clin N Am. 2012 Jan;23(1):7-13. Holekamp TF, Mollman ME, Murphy RK, et al. Dural arteriovenous fistula-induced thalamic dementia: report of 4 cases. J Neurosurg. 2016;124(6):1752-1765. Kim WY, Kim JB, Nam TK, Kim YB, Park SW. Cervical Myelopathy Caused by TE D 6. Intracranial Dural Arteriovenous Fistula. Korean J Spine. 2016;13(2):67-70. 7. Katz JM, Shetty T, Gobin YP, Segal AZ. Transient aphasia and reversible major Chou CH, Lin JC, Hsueh CJ, Peng GS. A thrombophilic patient with a dural AC C 8. EP depression due to a giant sagittal sinus dural AV fistula. 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LEGENDS 10 Vinayagamani ACCEPTED MANUSCRIPT FIG 1(A-F): At the time of initial presentation, gradient MR image (A) and 3D VRT(Volume rendered technique) image (B) reveals right TS-SS DAVF with dilated venous system and two venous aneurysms (arrows) RI PT involving BVR(basal vein of Rosenthal) with no mass effect. 3D TOF (Time of flight) angiography oblique axial and sagittal images (C,D) demonstrates the location of fistula (white arrows). A repeat CT (E) at the SC time of neurological deterioration shows hyperdensity in the left thalamic region (arrow) with perilesional edema. Axial FLAIR(Fluid attenuation M AN U inversion recovery) (F) shows venous aneurysm containing central flow void surrounded by well defined peripheral hyperintensity with thin hypointense rim suggestive of peripheral thrombosis (short arrow). Perianeurysmal edema (long arrow) involving thalamus and internal EP TE D capsule is also seen. FIG 2(A-F) :A-C Right external carotid artery (ECA) injection (Lateral AC C &AP view) confirms right transverse sinus-sigmoid sinus DAVF fed by petrosquamosal and basal tentorial branches (arrows) of right MMA with retrograde flow into posterior part of superior sagittal sinus and straight sinus. Note predominant reflux into BVR and cortical veins (arrows in B &C). D: 3D rotational angiography reconstructed in oblique sagittal plane shows venous aneurysms (arrows) of BVR at acute bends in its second and third segment(arrows in D). E: Check angiogram after initial stage onyx 11 Vinayagamani ACCEPTED MANUSCRIPT embolization shows significant reduction of venous reflux /shunt into deep veins. F: Follow up axial FLAIR image shows significant reduction in size of venous aneurysm with resolution of mass effect & edema (arrow). RI PT FIG3(A-C): Check angiogram of bilateral ECA(A,B) after second sitting embolization shows significant obliteration of fistula. (C) Unsubstracted image shows extensive onyx cast in the transverse sinus and torcula region. SC FIG(4A,B) : Schematic diagram showing DAVF illustrating probable pathophysiology of development of venous aneurysm in the index case. M AN U Shaded areas in A represents possible site of hemodynamic stress at curvatures. (arrows indicate the direction of flow) (1)- external carotid artery;(2)-middle meningeal artery; (3) -transverse sinus ; (4)- straight AC C EP Rosenthal) TE D sinus ; (5)- vein of galen ; (6) -internal cerebral vein; (7)- basal vein of 12 B C AC C EP TE D A M AN U SC RI PT ACCEPTED MANUSCRIPT D E F D M AN U B C EP TE D A AC C SC RI PT ACCEPTED MANUSCRIPT E F EP B AC C A TE D M AN U SC RI PT ACCEPTED MANUSCRIPT C AC C EP TE D M AN U SC RI PT ACCEPTED MANUSCRIPT A B ACCEPTED MANUSCRIPT HIGHLIGHTS • Our case illustrates a very rare and dynamic clinical manifestations of dural arteriovenous fistula (DAVF). RI PT • Episodic mass effect from venous aneurysm can cause predominant thalamic symptoms, presenting as recurrent transient subcortical thalamic aphasia, thalamic pain, hemiplegia and hemisensory loss. • Thalamic aphasia can rarely mimic transcortical variety possibly due to SC involvement of pulvinar and paramedian thalamic nuclei • Preferential arterialised flow into basal vein of Rosenthal can result in formation. M AN U increased hemodynamic stress at the acute bends and results in aneurysmal • Embolization of the DAVF could potentially reverse this unusual AC C EP TE D neurological condition. ACCEPTED MANUSCRIPT ABBREVIATIONS 2. BVR : Basal Vein of Rosenthal 3. MRI : Magnetic Resonance Imaging 4. DSA : Digital Substraction Angiography 5. MMA : Middle Meningeal Artery 6. ICA : Internal Carotid artery AC C EP TE D M AN U SC 7. TS-SS : Transverse sinus – Sigmoid Sinus RI PT 1. DAVF : Dural Arteriovenous Fistula