Fatal progression of posttraumatic dural arteriovenous fistulas refractory to multimodal therapy

Transcription

1 See the Letter to the Editor and the Response in this issue in Neurosurgical Forum, pp J Neurosurg 94: , 2001 Fatal progression of posttraumatic dural arteriovenous fistulas refractory to multimodal therapy Case report JONATHAN A. FRIEDMAN, M.D., FREDRIC B. MEYER, M.D., DOUGLAS A. NICHOLS, M.D., ROBERT J. COFFEY, M.D., L. NELSON HOPKINS, M.D., CORMAC O. MAHER, M.D., IRENE D. MEISSNER, M.D., AND BRUCE E. POLLOCK, M.D. Departments of Neurologic Surgery, Neurology, and Diagnostic Radiology, Mayo Clinic, Rochester, Minnesota; and Department of Neurosurgery and Toshiba Stroke Research Center, State University of New York at Buffalo School of Medicine and Biomedical Sciences, Buffalo, New York The authors report the case of a man who suffered from progressive, disseminated posttraumatic dural arteriovenous fistulas (DAVFs) resulting in death, despite aggressive endovascular, surgical, and radiosurgical treatment. This 31-year-old man was struck on the head while playing basketball. Two weeks later a soft, pulsatile mass developed at his vertex, and the man began to experience pulsatile tinnitus and progressive headaches. Magnetic resonance imaging and subsequent angiography revealed multiple AVFs in the scalp, calvaria, and dura, with drainage into the superior sagittal sinus. The patient was treated initially with transarterial embolization in five stages, followed by vertex craniotomy and surgical resection of the AVFs. However, multiple additional DAVFs developed over the bilateral convexities, the falx, and the tentorium. Subsequent treatment entailed 15 stages of transarterial embolization; seven stages of transvenous embolization, including complete occlusion of the sagittal sinus and partial occlusion of the straight sinus; three stages of stereotactic radiosurgery; and a second craniotomy with aggressive disconnection of the DAVFs. Unfortunately, the fistulas continued to progress, resulting in diffuse venous hypertension, multiple intracerebral hemorrhages in both hemispheres, and, ultimately, death nearly 5 years after the initial trauma. Endovascular, surgical, and radiosurgical treatments are successful in curing most patients with DAVFs. The failure of multimodal therapy and the fulminant progression and disseminated nature of this patient s disease are unique. KEY WORDS dural arteriovenous fistula trauma intracerebral hemorrhage endovascular therapy radiosurgery D URAL AVFs are believed to be acquired lesions that can occur as a result of head trauma. 1,6,7,10,16 Recently, stereotactic radiosurgery in combination with transarterial embolization has been shown to be effective for select patients with low-risk DAVFs, 18 especially for those in whom the fistulas involve the cavernous sinus. 26 Surgical disconnection of the abnormal arteriovenous communication, sometimes in combination with resection of an involved venous sinus, remains the gold standard for treatment of high-risk DAVFs and lesions refractory to endovascular therapy. 27 Aggressive clinical behavior of DAVFs is unusual. We report a case of a 31-year-old man with fulminant progression of multiple DAVFs that developed after he had experienced minor head trauma. Abbreviations used in this paper: AVF = arteriovenous fistula; CT = computerized tomography; DAVF = dural AVF; ECA = external carotid artery; ICA = internal carotid artery; MR = magnetic resonance; SSS = superior sagittal sinus; VA = vertebral artery. Case Report History. A previously healthy 31-year-old man was playing basketball when he was struck on the vertex by the palm of another player s hand. The man experienced a stinging sensation at the site of the impact that resolved over 3 minutes. There was no loss of consciousness and he continued to play without difficulty. Over the following 6 months, he noticed the development of a soft, bruised area at the site of impact and experienced pulsatile tinnitus bilaterally and intermittent headaches. Examination. The patient first presented for evaluation 1 year after the trauma and was found to have a pulsatile, 3-cm midline mass at the vertex, with nearby bluish discoloration, distention, and pulsatility over a radius of 6 cm of the adjacent scalp. There was marked enlargement of the superficial temporal arteries bilaterally, with bilateral CA bruits. The remainder of the patient s neurological examination was normal. Computerized tomography scans demonstrated a mid- 831

2 J. A. Friedman, et al. FIG. 1. Angiograms. Left: Lateral view (left internal maxillary artery injection) demonstrating multiple feeding arteries supplying a DAVF near the midline. Right: Lateral view (right ICA injection) demonstrating an enlarged branch of the meningohypophyseal trunk supplying a tentorial DAVF. line bone defect at the vertex with vascular grooves surrounding it. The SSS was markedly enlarged. Magnetic resonance imaging revealed diffuse flow voids involving the scalp and the posterior parietal calvaria in the midline, which traversed the outer table, diploic space, and inner table. There was no evidence of intracerebral hemorrhage or venous edema within the brain parenchyma. Cerebral angiography (Fig. 1 left) revealed a diffuse scalp AVF at the vertex, which drained into the SSS, and a large parietooccipital DAVF spanning the midline, which was fed predominantly by arterial branches from both ECAs and muscular branches from both VAs. Venous drainage was anterograde through the SSS, beginning at its middle segment, without evidence of cortical venous drainage. The left transverse sinus was occluded. A small tentorial DAVF was fed by a tentorial branch of the right meningohypophyseal trunk (Fig. 1 right). Treatment. The patient was treated with transarterial embolization of the fistula in five stages over a 1-month period. This embolization was followed by surgical excision of the scalp malformation, biparietal craniotomy, and disconnection of the DAVFs on both sides of the SSS. Follow-up cerebral angiograms demonstrated obliteration of the scalp lesion and the midparietal DAVF but a persistent DAVF located posteriorly over both the convexities and the falx, which was fed by branches of the right and left ECAs and both VAs. The tentorial DAVF on the right side was larger, and a new DAVF was now present in the region of the right jugular bulb and was fed by branches of the right VA. The patient underwent two additional transarterial embolizations. Three months later, the patient s scalp had normalized, but he experienced frequent headaches associated with nausea and vomiting. Magnetic resonance imaging (Fig. 2 upper left) revealed a subacute hemorrhagic infarction measuring 1 cm in the left lateral cerebellar hemisphere, without mass effect. Cerebral angiography (Fig. 2 upper right and lower left and right) revealed enlargement of the DAVFs located over the convexities, extending from the vertex posteriorly along the SSS and the falx, to the torcular herophili. Branches of the anterior and middle cerebral arteries bilaterally were now feeding the fistulous connections. There was anterograde flow posterior to the middle third of the SSS, retrograde flow anterior to FIG. 2. Upper Left: Axial T 2 -weighted MR image revealing left cerebellar hemorrhage. Upper Right: Anteroposterior angiogram (left ICA injection) demonstrating a DAVF of the SSS with some arterial supply from the middle and anterior cerebral arteries. Lower Left: Lateral angiogram (right internal maxillary artery injection) demonstrating multiple DAVFs with occlusion of a segment of SSS. Lower Right: Anteroposterior angiogram (left occipital artery injection) demonstrating multiple DAVFs within the posterior fossa. the SSS, and bilateral cortical venous drainage of both hemispheres, with drainage into the cavernous sinus and transverse sinuses through the vein of Labbé. The left transverse sinus was reconstituted, but was markedly narrowed. Stagnant flow of contrast material, diffusely apparent during the venous phase, indicated significant venous hypertension. A large left-sided DAVF within the posterior fossa was also identified. The patient underwent stereotactic radiosurgery in three stages to treat five separate DAVFs over a 3-month period. During the first procedure, fistulas of the SSS supplied by the left ECA (24.8 cm 3 ) and the tentorium (3.3 cm 3 ) were irradiated with margin doses of 15 Gy and 20 Gy, respectively. The second radiosurgical session was directed at the torcular herophili region. A radiation dose of 15 Gy to the margin was used to cover a volume of 7.8 cm 3. The third radiosurgery covered the posterior SSS as well as the DAVF located over the left parietal region. The margin dose was 16 Gy and the treated volume was 17.5 cm 3. Following the last radiosurgical procedure, the patient underwent five additional sessions of transarterial embolizations over a 3-month period. The patient continued to have headaches and pulsatile tinnitus but was otherwise well. Head CT scans (Fig. 3 left) obtained 6 months later (2.5 years after the initial trauma) demonstrated biparietal hypodensities extending to the posterior frontal lobe on the right side, which were consistent with edema. Repeated cerebral angiography (Fig. 3 center and right) revealed 832

3 Posttraumatic dural arteriovenous fistula FIG. 3. Left: A CT scan demonstrating biparietal hypodensities that are consistent with worsening venous edema. Center: Anteroposterior angiogram (left ICA injection) demonstrating bilateral convexity DAVFs. Right: Lateral angiogram (left VA injection) demonstrating DAVFs located at the tentorium, falx, transverse sinus, and jugular bulb. enlargement of the DAVF that was located over the middle and posterior SSS and the falx, which extended over the cerebral convexities bilaterally. Multiple DAVFs now involved the torcular herophili, right sigmoid sinus, and jugular foramen down to the posterior rim of the foramen magnum. Also noted was an increase in arteriovenous shunting, with a corkscrew appearance of the cortical veins, which was consistent with worsening venous hypertension. No anterograde flow through the torcular herophili was identified, in spite of normal patency and caliber of both transverse and sigmoid sinuses. The patient was treated with additional transarterial embolization in nine stages and transvenous embolization in seven stages over a 3-month period, including transvenous occlusion of the SSS in the fistulous region and partial transvenous occlusion of the straight sinus. However, CT scans demonstrated progressive venous edema in both parietal and occipital lobes, extending into the posterior frontal and posteromedial temporal lobes on the right side. A new left convexity fistula was observed to drain in a retrograde direction through cortical veins into the anterior SSS. The patient remained neurologically intact, but experienced worsening headache and vomiting, indicative of raised intracranial pressure. Three years after the initial trauma, the patient underwent a parasagittal craniotomy, and the left convexity DAVF was resected without complication. Cerebral angiography (Fig. 4) performed 3 months later (3.25 years after the initial trauma) demonstrated resolution of the left convexity lesion, but the appearance of a new right tentorial DAVF that was fed by the superior cerebellar artery and drained into the vein of Galen. This was associated with retrograde venous drainage into the basal veins of Rosenthal bilaterally. Attempted embolization of this right tentorial DAVF was complicated by perforation of the basilar artery, which was treated by an endovascular balloon tamponade, followed by external ventricular drainage. The patient s course was complicated by pseudomonal ventriculitis, from which he made a complete recovery and returned home. Two months later MR imaging revealed persistent venous edema bilaterally, with some enhancement in the superior occipital lobes bilaterally that was consistent with radiation-induced change. No further treatment was recommended at that time. Posttreatment Course. The patient remained cognitively intact, but experienced persistent headaches and decreasing visual acuity, which progressed to legal blindness. Four years after the initial trauma, the patient experienced a generalized tonic clonic seizure. Computerized tomography scanning (Fig. 5 left) revealed a 3.5-cm right parietal hemorrhage surrounded by extensive edema, with punctate hemorrhages in the right basal ganglia and corpus callosum. The patient was obtunded, but exhibited some purposeful movements, more so on the right side. Cerebral angiography (Fig. 5 right) revealed increased retrograde drainage through the basal cortical veins, retrograde venous drainage through the left vein of Labbé, and markedly slower drainage during the venous phase, which was consistent with worsened venous hypertension. A previously noted large cortical vein over the right parietal region, which drained in a retrograde direction from the SSS to the sphenoparietal sinus, was no longer visualized and may have played a causal role in the patient s right parietal hemorrhage. The patient was extubated, but had markedly diminished mentation and a mild left hemiparesis. After discussion with the patient s family, given the relentless progression of the disease in spite of aggressive management, no further surgical or endovascular interventions were offered. Serial CT scans demonstrated persistent, diffuse, bilateral venous edema. The patient experienced ongoing seizures, which were difficult to control, and recurrent aspiration pneumonia. A tracheostomy was performed and FIG. 4. Left: Lateral angiogram (left VA injection, late arterial phase) demonstrating many diffuse DAVFs. Multiple intravascular platinum coils can be seen. Right: Lateral angiogram (left VA injection, late venous phase) demonstrating retrograde venous drainage into a dilated, corkscrewlike basal vein of Rosenthal. 833

4 J. A. Friedman, et al. FIG. 5. Left: A CT scan demonstrating right parietal hemorrhage with an intravascular coil artifact. Right: Lateral angiogram (left VA injection, late venous phase) demonstrating disseminated posterior fossa DAVFs with delayed, retrograde venous drainage and dilated, corkscrewlike veins. a percutaneous gastric feeding tube was placed. His level of consciousness fluctuated, but never substantially improved. The patient died of pneumonitis 4.75 years after the initial trauma. Discussion Although some DAVFs may be congenital, typically they are acquired lesions that occur as a result of trauma, surgical procedure, or venous sinus thrombosis. 7,13,19 Surgical excision or disconnection has been the traditional treatment used for DAVFs and is usually definitive. 27 Recently, transarterial and transvenous embolization, often in combination with radiosurgery, have been demonstrated to be effective primary treatments for certain DAVFs, although some lesions persist after this treatment. 12,18,21 Both surgical and endovascular procedures have been used in complex cases with good success. In several series conducted by Barnwell and colleagues, 2,3 and in one conducted by Pelz, et al., 25 no treatment failures were reported. In the case described here, aggressive multimodal therapy not only was unsuccessful in eradicating the disease, but the DAVFs progressed and, ultimately, led to the patient s death. Both atypical and complex DAVFs have been described. 2,3,23,29 Nakamura and colleagues 23 reported on two patients with multiple DAVFs, who presented with symptoms of raised intracranial pressure. Barnwell and colleagues 3 reported their results with 16 large or complicated DAVFs. In both of these reports, treatment was successful in obliterating the fistula, with no deaths. In neither report was a disseminating, expansive pattern of DAVFs described. The natural history of DAVFs is variable. 1 Spontaneous disappearance on angiography has been described, and some patients will have benign symptomatology. 4,7,15,24 Some DAVFs do behave aggressively, and risk factors for an aggressive neurological course and hemorrhage have been established. 1,6,8,14,20 Fatal intracerebral hemorrhage can occur. 1,6,9,16 Progression of DAVFs has also been described, and these lesions are known to recruit small feeding arteries over time. 1,9 Our patient s disease progressed dramatically to involve multiple dural sinuses and both convexities, with associated cortical venous drainage and venous hypertension in both hemispheres. It seems likely that this patient had an underlying predisposition to the formation of DAVFs and their enlargement. Angiogenic factors have been proposed to be important in the pathophysiology of DAVFs, and individual differences in the expression or pathological overexpression of these factors may explain a genetic propensity to form the lesions. 17 Individual variation of venous anatomy and/or venous drainage pattern might also have predisposed our patient to severe venous hypertension, particularly if a major venous outflow channel was transiently occluded as a result of the trauma. In this case, we observed the left transverse sinus to be occluded on the initial angiogram and it reconstituted to normal caliber over time. It is also possible that this patient had one or more preexisting, subclinical DAVFs, with a dramatic exacerbation of the disease process following minor trauma. Even if this were the case, the fulminant progression and failure of multimodal treatment are noteworthy. The origin of DAVFs has been controversial, but a consensus has emerged that DAVFs form as a result of acquired abnormalities of venous drainage. 13,21,22 In the clinical setting, this is most commonly the result of focal venous sinus thrombosis. This hypothesis has been supported by data from laboratory and clinical investigations implicating venous hypertension as a key component of the underlying pathophysiology of the formation of DAVFs. 17,28 Angiogenic factors have been implicated in this process. 17 One possible mechanism is that chronic venous hypertension may dilate the venous end of dural capillaries, ultimately causing ectatic dilation of the entire capillary network and precipitating direct arteriovenous connections. 11,28 This is analogous to the formation of mucosal arteriovenous malformations in the gastrointestinal tract, which are thought to occur by a similar mechanism. 5 Venous hypertension is a consequence of DAVFs that may worsen as the flow through the fistula increases. If venous hypertension also plays a causal role in the formation of new DAVFs, it is possible that the progressive venous hypertension of this patient s initial lesion may have induced the formation of new DAVFs. This cycle may perpetuate itself; that is, as DAVFs enlarge and new ones form, venous hypertension increases, leading to additional DAVF enlargement and formation, and so forth. Although this may explain the disease progression in our patient, this is clearly not a pattern typical of most patients with DAVFs, even those with clear evidence of cortical venous drainage and venous hypertension. In this patient the protracted, piecemeal multimodal therapy that was used not only was ineffective, but also was associated with progressively intractable and, ultimately, fatal intracranial venous hypertension. After the failure of the first surgery, an aggressive attempt at repeated surgical disconnection earlier in the course of the disease may have been more successful in this case, because the entire lesion could not be rapidly and completely treated with radiosurgery and embolization. Conclusions We have described a patient with fulminant posttraumatic DAVFs, in whom there was fatal progression of the 834

5 Posttraumatic dural arteriovenous fistula lesions, in spite of aggressive multimodal treatment. The progression of disease in this case indicates that genetic or angiogenic factors may predispose select patients with DAVFs to additional fistula formation and a more aggressive clinical course. Acknowledgment The authors are indebted to Mary Soper for her assistance with manuscript preparation and reproduction of figures. References 1. Awad IA, Little JR, Akarawi WP, et al: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72: , Barnwell SL, Halbach VV, Dowd CF, et al: A variant of arteriovenous fistulas within the wall of dural sinuses. Results of combined surgical and endovascular therapy. J Neurosurg 74: , Barnwell SL, Halbach VV, Higashida RT, et al: Complex dural arteriovenous fistulas. Results of combined endovascular and neurosurgical treatment in 16 patients. J Neurosurg 71: , Bitoh S, Sakaki S: Spontaneous cure of dural arteriovenous malformation in the posterior fossa. Surg Neurol 12: , Boley SJ, Sammartano R, Adams A, et al: On the nature and etiology of vascular ectasias of the colon. Degenerative lesions of aging. Gastroenterology 72: , Brown RD Jr, Wiebers DO, Nichols DA: Intracranial dural arteriovenous fistulae: angiographic predictors of intracranial hemorrhage and clinical outcome in nonsurgical patients. J Neurosurg 81: , Chaudhary MY, Sachdev VP, Cho SH, et al: Dural arteriovenous malformation of the major venous sinuses: an acquired lesion. AJNR 3:13 19, Cognard C, Gobin YP, Pierot L, et al: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194: , Enker SH: Progression of a dural arteriovenous malformation resulting in an intracerebral hematoma. A case report. Angiology 30: , Freckmann N, Sartor K, Herrmann HD: Traumatic arteriovenous fistulae of the middle meningeal artery and neigbouring veins or dural sinuses. Acta Neurochir 55: , Friedman JA, Pollock BE, Nichols DA: Development of a cerebral arteriovenous malformation documented in an adult by serial angiography. Case report. J Neurosurg 93: , Halbach VV, Higashida RT, Hieshima GB: Dural fistulas involving the transverse and sigmoid sinuses: results of treatment in 28 patients. Radiology 163: , Houser OW, Campbell JK, Campbell RJ, et al: Arteriovenous malformation affecting the transverse dural venous sinus an acquired lesion. Mayo Clin Proc 54: , Ishii K, Goto K, Ihara K, et al: High-risk dural arteriovenous fistulae of the transverse and sigmoid sinuses. AJNR 8: , Kataoka K, Taneda M: Angiographic disappearance of multiple dural arteriovenous malformations. Case report. J Neurosurg 60: , Lasjaunias P, Chiu M, Ter Brugge K, et al: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64: , Lawton MT, Jacobowitz R, Spetzler RF: Redefined role of angiogenesis in the pathogenesis of dural arteriovenous malformations. J Neurosurg 87: , Link MJ, Coffey RJ, Nichols DA, et al: The role of radiosurgery and particulate embolization in the treatment of dural arteriovenous fistulas. J Neurosurg 84: , Morioka T, Nishio S, Hikita T: Traumatic arteriovenous fistulae of the scalp at the area of previous craniotomy. Surg Neurol 30: , Morita A, Meyer FB, Nichols DA, et al: Childhood dural arteriovenous fistulae of the posterior dural sinuses: three case reports and literature review. Neurosurgery 37: , Mullan S: Reflections upon the nature and management of intracranial and intraspinal vascular malformations and fistulae. J Neurosurg 80: , Mullan S, Mojtahedi S, Johnson DL, et al: Cerebral venous malformation arteriovenous malformation transition forms. J Neurosurg 85:9 13, Nakamura M, Tamaki N, Hara Y, et al: Two unusual cases of multiple dural arteriovenous fistulas. Neurosurgery 41: , Obrador S, Soto M, Silvela J: Clinical syndromes of arteriovenous malformations of the transverse-sigmoid sinus. J Neurol Neurosurg Psychiatry 38: , Pelz DM, Lownie SP, Fox AJ, et al: Intracranial dural arteriovenous fistulae with pial venous drainage: combined endovascular-neurosurgical therapy. Can J Neurol Sci 24: , Pollock BE, Nichols DA, Garrity JA, et al: Stereotactic radiosurgery and particulate embolization for cavernous sinus dural arteriovenous fistulae. Neurosurgery 45: , Sundt TM Jr, Piepgras DG: The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg 59:32 39, Terada T, Higashida RT, Halbach VV, et al: Development of acquired arteriovenous fistulas in rats due to venous hypertension. J Neurosurg 80: , Viñuela F, Fox AJ, Pelz DM, et al: Unusual clinical manifestations of dural arteriovenous malformations. J Neurosurg 64: , 1986 Manuscript received August 23, Accepted in final form January 3, Address reprint requests to: Jonathan A. Friedman, M.D., Department of Neurologic Surgery, Joseph 1-229, Saint Mary s Hospital, 1216 Second Street SW, Rochester, Minnesota friedman.jonathan@mayo.edu. 835