p024 p.1 [100%]

Neurol Med Chir (Tokyo) 44, 24¿28, 2004

Intracranial Dural Arteriovenous Fistula With Venous Reflux to the Brainstem and Mimicking Brainstem —Case Report—

Jun LI*,#, Masayuki EZURA**,AkiraTAKAHASHI**,andTakashiYOSHIMOTO***

*Department of Neuroendovascular Therapy, Kohnan Hospital, Sendai, Miyagi; Departments of **Neuroendovascular Therapy and ***Neurosurgery, Tohoku University School of Medicine, Sendai, Miyagi; #Department of , Qingdao Municipal Hospital, Qingdao, P.R.C.

Abstract

A 73-year-old man presented with a rare transverse sinus dural arteriovenous fistula (dAVF) with venous reflux to the brainstem and medulla manifesting as brainstem and spinal cord edema mimicking brainstem infarction. Complete occlusion of the fistula was achieved by transvenous embolization, resulting in angiographic cure of the fistula and progressive improvement of the symptoms. Intracrani- al dAVFs with perimedullary venous drainage, type V according to the Cognard classification, are rare lesions with distinctive clinical, radiological, and therapeutic aspects. This case demonstrates that the symptoms of dAVF with perimedullary venous reflux are variable, so dAVF should be considered in patients with clinical and radiological findings suggestive of congestion in the brainstem and spinal cord. Dysfunction of the medulla and spinal cord caused by venous hypertension is the most probable cause of the neurological symptoms in such cases. Interventional therapy can lead to angiographic cure and resolution of the symptoms.

Key words: dural arteriovenous fistula, vascular , venous hypertension, embolization

Introduction We present a rare case of transverse sinus dAVF with venous reflux to the brainstem and medulla Dural arteriovenous fistulae (dAVFs) are character- manifesting as brainstem and spinal cord edema ized by abnormal shunting of blood between the mimicking brainstem infarction. arterial system (meningeal branches and rarely cortical branches of the external and internal Case Report carotid and vertebral arteries) and the venous system (dural sinus or close structures), without the A 73-year-old man developed dizziness, nausea, presence of a normal intervening bed. vomiting, and progressive motor weakness in the

dAVFs account for 10% to 15% of all intracranial bilateral lower extremities within 3 days. T2-weight- arteriovenous malformations (AVMs).1) Spinal ed magnetic resonance (MR) imaging revealed a dAVF with perimedullary venous drainage is a well- hyperintense area in the pontomedullary region, as known cause of vascular myelopathy. However, well as a hyperintense area in the left temporal lobe, intracranial dAVF with venous drainage into the which was not identified at that time (Fig. 1). He spinal is far less common and may be associ- had no significant medical history. One week later,

ated with myelopathy. The diagnosis of this uncom- T2-weighted MR imaging showed a hyperintense mon type of drainage is usually challenging because area in the left temporal lobe. He was treated under a the presenting symptoms are variable and often diagnosis of acute cerebral infarction. The patient related to dysfunction of the spine, rather than the was discharged with right leg paresis. Three months brain. later, the patient suddenly developed quadriplegia, unconsciousness, and dyspnea. Brain MR imaging Received April 18, 2003; Accepted August 27, 2003 revealed no new lesion. The diagnosis was recur-

24 p024 p.2 [100%]

Type V dAVF Mimicking Brainstem Infarction 25

Fig. 1 Axial fluid-attenuated inversion recovery Fig. 2 Serial sagittal T2-weighted magnetic magnetic resonance images at the initial resonance images in the cervical plane, 7 onset showing hyperintense areas (arrow)in months (A), 8 months (B), and 11 months the medulla oblongata (A) and left temporal after onset (C), and 5 days after emboliza- lobe (B). tion (D), showing changes in the size of the hyperintense area (arrow) with time. Note the obvious shrinkage of the hyperintense lesion and disappearance of the flow void rence of acute cerebral infarction. The patient was ahead and beyond the medulla oblongata 5 intubated and ventilated and given ischemic ther- days after embolization. apy. He gradually regained consciousness. After rehabilitation, he was discharged with bowel and bladder dysfunction and confined to a wheelchair. through a microcatheter (Transit II; Cordis Co., Comparison of the serial MR images revealed that Miami, Fla., U.S.A.) via the retrograde left internal the size and density of lesions in the medulla and jugular approach. Postembolization an- temporal lobe changed with time. MR imaging also giography showed angiographic cure of the fistula revealed hyperintensity from the medulla to the level (Fig. 3D, E). of C-5, and a flow void (Fig. 2A–C). AVM was After the interventional therapy, the patient's suspected. He was referred to our hospital one year neurological status progressively improved, and MR after the initial onset. imaging revealed obvious shrinkage of the hyperin- On admission, the patient had clear consciousness tensity 5 days after the therapy (Fig. 2D). and no cranial nerve disturbance. He had normal strength in the upper extremities, but severe Discussion weakness in the proximal lower extremities. The deep- reflexes were normal in both arms and Only a few cases of intracranial dAVF with hyperactive in the legs. Babinski's reflex was present spinal perimedullary venous drainage have been bilaterally. Pinprick sensation was decreased in the reported.2–4,6–8,10,15–17,19–30) The most common symp- S-2 dermatome. Cerebral demonstrated tom is ascending myelopathy, starting as loss of a dAVF in the left transverse sinus, type V according sensationandmotorfunctioninthelowerextremi- to the Cognard classification, fed by the left middle ties and extending to the upper extremities. Sphinc- meningeal artery and meningeal branches of the ter function is impaired. Brainstem symptoms are occipital artery, and drained by the ipsilateral sig- the last to appear and are related to the pattern of moid sinus, jugular vein, and anterior and posterior the venous drainage, which involves the anterior spinal veins (Fig. 3A–C). There was severe stenosis pontomesencephalic vein.8) Review of 37 cases in the left sigmoid sinus. In addition, the meningeal concluded that the symptoms are usually progres- branch from the right ascending pharyngeal artery sive (28 of 37 cases), but acute onset of neurological acted as a feeder across the midline to the left disorders occurs in 25% of cases (8 of 37 cases). transverse sinus. Bulbar dysfunction was reported in seven cases.22) Endovascular embolization was selected as The neurological symptoms of our patient were treatment. Complete occlusion of the fistula was most likely related to spinal cord dysfunction (bowel achieved by transvenous embolization of the trans- and bladder dysfunction and paraparesis) as well as verse sinus using interlocking detachable coils brainstem signs such as unconsciousness and (Boston Scientific, Boston, Mass., U.S.A.) delivered dyspnea. The symptoms of our patient are similar to

Neurol Med Chir (Tokyo) 44, January, 2004 p024 p.3 [100%]

26 J. Li et al.

Fig. 3 A: Left external carotid angiogram, lateral view, showing two shunts from the middle menin- geal artery to the transverse sinus (arrows), and one shunt from the occipital artery to the transverse sinus (curved arrow). B: Selective angiogram of the left occipital artery, lateral view, showing cortical vein reflux through the vein of Labb áe to the sylvian vein (arrow)and severe stenosis in the left transverse sinus (arrowhead). C: Lateral view of the left occipital artery, late phase, showing anterior and posterior spinal vein reflex (arrows). D: Postopera- tive left external carotid angiogram showing the angiographic cure of the fistula. E: Radio- graph of the brain, lateral view, showing coils filling the transverse sinus (arrow).

those of previously reported cases of intracranial symptoms is spinal cord venous hypertension. The dAVFs, in which the patients presented with my- high pressure of retrograde arterial flow into the elopathy first and brainstem symptoms appeared venous systems is thought to be an important cause later. However, the acute onset of the symptoms and of venous . The severe stenosis of the trans- hyperintensity in the pontomedullary region led to verse sinus was the likely cause of the retrograde an incorrect initial diagnosis. venous drainage into the vein of Labb áe and the Spinal cord dysfunction has several causes14): anterior pontomesencephalic and spinal perimedul- diversion or ``stealing'' of blood from the spinal lary veins. Therefore, a transverse sinus dAVF may cord, cord compression by dilated vascular struc- result in spinal cord venous hypertension, thus tures, hemorrhage, and chronic venous hyperten- behaving exactly like dAVFs that drain directly into sion within the spinal cord. Spinal cord ischemia the spinal veins.9) Ourcaseisagoodexampleofthis caused by arterial steal could be excluded in this phenomenon. case because of the low-flow fistula, and the external Venous congestion in the spinal cord and brain- carotid artery does not supply the spinal cord. No stem of our patient may have been caused by trans- cord compression, hemorrhage, or spontaneous verse sinus AVF reflux to the anterior and posterior were detected in this patient. The only spinal veins via well-described anastomotic venous possible mechanism for the neurological deficit is channels. The anterior spinal vein is continuous venous congestion and secondary cord swelling, superiorly with the anterior medullary vein, which which is supported by the enlargement and hyperin- in turn communicates with the anterior pon- tensity observed in the brainstem and cervical cord tomesencephalic vein and so the petrosal vein. The by MR imaging. posterior spinal vein is continuous superiorly with The pathophysiologic mechanism of the spinal the vein of the restiform body and/or the retroolivary

Neurol Med Chir (Tokyo) 44,January,2004 p024 p.4 [100%]

Type V dAVF Mimicking Brainstem Infarction 27

vein,12) so the drainage of the fistula to the spinal There is general agreement that embolization cord produces elevated pressure in the coronal should be attempted first, and reserved for venous plexus or the medullary veins, thus causing a lesions that are incompletely occluded or recur after decrease in the arteriovenous pressure gradient and embolization.13) Interruption of the vein draining the ischemia. Radioanatomic studies have demonstrat- fistula into the spinal cord venous system is proba- ed anastomoses between the pontomesencephalic bly adequate. Our case demonstrates that interrup- system and the spinal medullary veins, but such tion of the cranial dural fistula draining into spinal anastomoses may become active only after initiation veins can achieve angiographic cure and resolution such as intracranial thrombosis or arteriovenous of the symptoms. shunting.2) Theangiographicfindingswerecorrelatedwith Acknowledgments clinical presentations of dural AVMs and showed that the symptoms are related to the venous charac- This study was supported in part by the Japan-China ter and depend on the territory of the draining veins Sasakawa Medical Fellowship in 2002, and present- of the dural AVMs.11,18) Six of a series of 12 patients ed in part in abstract format at the Fifth Meeting of with type V dAVFs had myelopathy with slow-flow the Asian-Australasian Federation of Interventional spinal perimedullary venous drainage that extended & Therapeutic Neuroradiology (November 2002, to the thoracic or lumbar spinal cord.5) The other six Hong-Kong). patients without myelopathy (five with hemor- rhages, one with focal neurological deficit) had References spinal venous drainage limited to the cervical cord, as a cervical radiculomedullary vein drained the 1) Barnwell SL, Halbach VV, Higashida RT, Hieshima arterialized flow from the dAVF into the epidural G, Wilson CB: Complex dural arteriovenous fistulas. space. This type of drainage is thought to prevent Results of combined endovascular and neurosurgical spinal cord venous hypertension and myelopathy. treatment in 16 patients. J Neurosurg 71: 352–358, The symptoms of our patient were probably caused 1989 2) Bret P, Salzmann M, Bascoulergue Y, Guyotat J: by the venous drainage to the pontomesencephalic Dural arteriovenous fistula of the posterior fossa system as well as the spinal medullary veins, thus draining into the spinal medullary veins — an un- causing venous hypertension and both spinal and usual cause of myelopathy: case report. Neurosurgery brainstem signs. 35: 965–969, 1994 At the first presentation of our case, T2-weighted 3) Brunet E, Tache R, Lafitte F, Piotin M, Miaux Y, MR imaging revealed localized high intensity in the Martin-Duverneuil N, Chiras J: [Intracranial dural pontomedullary region and left temporal lobe. arteriovenous fistula with perimedullary venous However, this condition was not distinguished from drainage]. JNeuroradiol25: 103–110, 1998 (Fre, with cerebral infarction because of the acute onset, brain- Eng abstract) stem symptoms (dizziness, nausea, vomiting), and 4) Chen CJ, Chen CM, Lin TK: Enhanced cervical MRI the high intensity in the pontomedullary region. The in identifying intracranial dural arteriovenous fistulae with spinal perimedullary venous drainage. important points are first, the progressive motor Neuroradiology 40: 393–397, 1998 weakness in the bilateral lower extremities could not 5) Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, be explained by the lesion in the brainstem, and Casasco A, Chiras J, Merland JJ: Cerebral dural second, the lesions in the temporal lobe and the arteriovenous fistulas: clinical and angiographic pontomedullary region could not be explained by correlation with a revised classification of venous single vessel infarction. Serial MR imaging also drainage. Radiology 194: 671–680, 1995 demonstrated changes in the size and intensity of 6) Criscuolo GR, Oldfield EH, Doppman JL: Reversible the lesion in the pontomedullary region, which acute and subacute myelopathy in patients with dural could not be explained by infarction. In such a situa- arteriovenous fistulas. Foix-Alajouanine syndrome tion, dAVF should be considered and additional reconsidered. J Neurosurg 70: 354–359, 1989 MR angiography or digital subtraction angiography 7) Gaensler EH, Jackson DE Jr, Halbach VV: Ar- should be performed. Congestive regions appeared teriovenous fistulas of the cervicomedullary junction as a cause of myelopathy: radiographic findings in as hyperintense areas on the T -weighted MR images 2 two cases. AJNR Am J Neuroradiol 11: 518–521, 1990 and the draining vein as a flow void. The shrinkage 8) Gobin YP, Rogopoulos A, Aymard A, Khayata M, of the hyperintense pontomedullary lesion in the ReizineD,ChirasJ,MerlandJJ:Endovasculartreat- follow-up MR imaging studies suggests that reversi- ment of intracranial dural arteriovenous fistulas with ble edema rather than infarction was the cause of spinal perimedullary venous drainage. J Neurosurg the hyperintensity. 77: 718–723, 1992

Neurol Med Chir (Tokyo) 44, January, 2004 p024 p.5 [100%]

28 J. Li et al.

9) Graeh D, Dolman C: Radiological and pathological 22) Ricolfi F, Manelfe C, Meder JF, Arrue P, Decq P, aspects of dural arteriovenous fistulas. J Neurosurg Brugieres P, Cognard C, Gaston A: Intracranial dural 64: 962–967, 1986 arteriovenous fistulae with perimedullary venous 10) Hahnel S, Jansen O, Geletneky K: MR appearance of drainage. Anatomical, clinical and therapeutic con- an intracranial dural arteriovenous fistula leading to siderations. Neuroradiology 41: 803–812, 1999 cervical myelopathy. Neurology 51: 1131–1135, 1998 23) Rivierez M, Gazengel J, Chiras J, Dorwling-Carter D, 11) Houser O, Baker H, Rhoton A, Okazaki H: Intracrani- Debussche D, Dubbs M, Kanaan H: [Vertebro-dural al dural arteriovenous malformations. Radiology 105: arteriovenous fistulae of the foramen magnum with 55–64, 1972 perimedullary venous drainage]. Neurochirurgie 37: 12) Huang YP, Wolf BS: Veins of the posterior fossa, in 179–184, 1991 (Fre, with Eng abstract) Newton TH, Potts DG (eds): Radiology of the Skull and 24) Symon L, Kuyama H, Kendall B: Dural arteriovenous Brain, vol 2, book 3. St Louis, CV Mosby, 1974, pp malformations of the spine. Clinical features and 2155–2219 (see pp 2171–2181) surgical results in 55 cases. J Neurosurg 60: 238–247, 13) Javier RM, Kehrli P, Beaujeux R, Herr F, Sibilia J, 1984 Kuntz JL: A case of intracranial dural arteriovenous 25)VasdevA,LefournierV,BessouP,DematteisM, fistula draining into spinal medullary veins. Rev Crouzet G: [Intracranial dural fistula with spinal cord Rhum Engl Ed 66: 425–429, 1999 venous drainage. Apropos of 2 cases]. J Neuroradiol 14) Krayenbuhl H, Yasargil MG, McClintock HG: Treat- 21: 134–154, 1994 (Fre, with Eng abstract) ment of spinal cord vascular malformations by 26) Versari PP, D'Aliberti G, Talamonti G, Branca V, surgical excision. J Neurosurg 30: 427–435, 1969 Boccardi E, Collice M: Progressive myelopathy 15) Mahagne MH, Rogopoulos A, Paquis P, Guilhem D, caused by intracranial dural arteriovenous fistula: Lonjon M, Grellier P, Chatel M: [Intracranial dural report of two cases and review of the literature. arteriovenous fistula with spinal venous drainage]. Neurosurgery 33: 914–919, 1993 Rev Neurol (Paris) 148: 789–792, 1992 (Fre, with Eng 27) Wiesmann M, Padovan CS, Pfister HW, Yousry TA: abstract) Intracranial dural arteriovenous fistula with spinal 16) Manelfe C, Lasjaunias P, Halbach VV, Mark AS: medullary venous drainage. Eur Radiol 10: Embolization in the brain, in Dondelinger RF, Rossi 1606–1609, 2000 P, Kurdziel JC, Wallace S (eds): Interventional 28) Willinsky R, TerBrugge K, Lasjaunias P, Montanera Radiology. Stuttgart, Thieme, 1990, pp 396–420 W: The variable presentations of craniocervical and 17) Mascalchi M, Scazzeri F, Prosetti D, Ferrito G, cervical dural arteriovenous malformations. Surg Salvi F, Quilici N: Dural arteriovenous fistula at the Neurol 34: 118–123, 1990 craniocervical junction with perimedullary venous 29) Woimant F, Merland JJ, Riche MC, de Liege P, drainage. AJNR Am J Neuroradiol 17: 1137–1141, Bertrand HJ, Bacri D, Haguenau M, Pepin B: 1996 [Bulbospinal syndrome related to a meningeal 18) Obrador S, Soto M, Silvela R: Clinical syndromes arteriovenous fistula of the lateral sinus draining of arteriovenous malformations of the transverse into spinal cord veins]. Rev Neurol (Paris) 138: sigmoid sinus. J Neurol Neurosurg Psychiatry 38: 559–566, 1982 (Fre) 436–451, 1975 30) Wrobel CJ, Oldfield EH, Di Chiro G, Tarlov EC, 19) Partington MD, Rufenacht DA, Marsh WR, Piepgras Baker RA, Doppman JL: Myelopathy due to intra- DG: Cranial and sacral dural arteriovenous fistulae cranial dural arteriovenous fistulas draining intra- as a cause of myelopathy. J Neurosurg 76: 615–622, thecally into spinal medullary veins. J Neurosurg 69: 1992 934–939, 1988 20) Picard L, Bracard S, Islak C, Roy D, Moreno A, Marchal JC, Roland J: Dural fistulae of the tentorium cerebelli: radioanatomical, clinical and therapeutic considerations. J Neuroradiol 17: 161–181, 1990 (Eng Address reprint requests to:M.Ezura,M.D.,Departmentof and Fre) Neuroendovascular Therapy, Tohoku University 21) PierotL,ChirasJ,MederJF,RoseM,RivierezM, School of Medicine, 2–1 Seiryo–cho, Aoba–ku, Marsault C: Dural arteriovenous fistulas of the Sendai, Miyagi 980–8575, Japan. posterior fossa draining into subarachnoid veins. e-mail:ezu＠ivns.med.tohoku.ac.jp AJNR Am J Neuroradiol 13: 315–323, 1992

Neurol Med Chir (Tokyo) 44,January,2004