Intracranial Hypertension Associated with UnrupturedCerebral Arteriovenous Malformations Marc I. Chimowitz, MD," John R. Little, MD,t Issam A. Awad, MD,? Cathy A. Sila, MD," G. Kosmorsky, DO,$ and Anthony J. Furlan, MD" ~~
Only 6 patients with intracranial hypertension associated with unruptured cerebral arteriovenous malformations have been reported. We report 6 additional patients seen at the Cleveland Clinic during the past 10 years. The average age was 28 years (range, 19-44 years); 4 were women. Symptoms and signs included papilledema (6patients), headache (6), transient nonepileptic focal symptoms (4),visual obscurations (3,ipsilateral carotid or ocular bruits (3), abnormal visual fields (3), focal seizures (2), and progressive visual loss (1). Enhanced computed tomography (CT) or magnetic resonance imaging (MRI) demonstrated the malformations in all 6 patients. The malformations were large, supplied by the branches of the middle and anterior cerebral arteries, with the posterior cerebral artery contributing in 3 patients, and all drained into the superior sagittal sinus. Associated venous obstruction was seen in 2 patients. Four patients underwent excision of the arteriovenous malformation, with resolution of papilledema in all 4. Measurements of cortical arterial and venous pressures during surgery in 3 patients showed decreased feeding artery pressures and elevated draining vein pressures, which normalized after removal of the malformation. Treatment in the 2 remaining patients consisted of medical therapy (acetazolamide, furosemide, steroids) alone in 1 patient, and in conjunction with proton beam radiation in the other. Papilledema resolved in the former patient, but the patient receiving proton beam radiation still had papilledema 2 years later. Intracranial hypertension associated with unruptured cerebral arteriovenous malformations occurs in young patients with high flow malformations that drain into the superior sagittal sinus, and is likely the result of increased cortical venous and superior sagittal sinus pressure. Excision of the malformation effectively reduces the intracranial pressure. Chimowitz MI, Little JR, Awad IA, Sila CA, Kosmorsky G, Furlan AJ. Intracranial hypertension associated with unruptured cerebral arteriovenous malformations. Ann Neurol 1990;27:474-479
Intracranial hypertension is an uncommon presenta-
tion of unruptured cerebral arteriovenous malformations (AVMs). In a clinical survey of 110 intracranial angiomas reported in 1955, Paterson and McKissock briefly described 1 patient with an unruptured occipital angioma and papilledema [l). Since then only 6 patients have been reported [2-61. We report 6 additional patients with unruptured cerebral AVMs and intracranial hypertension; review the literature; and attempt to clarify the clinical, radiological, and pathophysiological features of this unusual entity.
Methods The 6 patients represent a nonconsecutive, selected group identified over a 10-year period (1979-1989) at the Cleveland Clinic. Evaluation of each patient included a neurological assessment by at least one of us, neuro-ophthalmological consultation with formal visual fields, cranial computed tomography (CT) or magnetic resonance imaging (MRI), and From the Departments of *Neurology, ?Neurosurgery, and SNeuroOphthalmology, Cleveland Clinic Foundation, Cleveland, OH. Received Jun 23, 1989, and in revised form Oct 27. Accepted for publication Oct 27, 1989.
three-vessel cerebral angiography. Four patients underwent complete microsurgical removal of the AVMs. These procedures were carried out under general anesthesia with the patient positioned supine. After dural opening, measurements of cortical arterial and venous pressures were carried out in 3 of the 4 patients. This technique was previously described in detail 17-31. A 26-gauge needle was coupled to a strain gauge transducer by semirigid fluid-filled tubing. All pressure transducers, including the one measuring the systemic arterial blood pressure, were leveled to the right atrium of the heart. The feeding artery pressure was measured before excision of the AVM by inserting the needle under microscopic visualization into a segment of the artery within 1 cm of the AVM margin. Draining vein pressure was then measured by inserting the needle into a major vein draining arteridzed blood within 1 cm of the AVM margin. Measurement of draining vein pressure was repeated after AVM excision. Outcome in all patients was closely monitored over periods ranging from 4 months to 10 years since initial diagnosis. An extensive review of the English literature yielded 6 Address correspondence to Dr Furlan, Department of Neurology, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195.
474 Copyright 0 1990 by the American Neurological Association
previously reported patients with unruptured cerebral AVMs and intracranial hypertension 12-61. Results Clinical Features Table 1 summarizes the clinical and radiological findings and outcome in our 6 patients. The average age of the 6 patients was 28 years (range, 19-44 years); 4 were women. Presenting symptoms included headache (6 patients); transient language, motor, or sensory symptoms (4); visual obscurations (3); focal seizures (2); and progressive bilateral visual loss (1). Signs included papilledema (6 patients), ipsilateral carotid or ocular bruits (3), and abnormal visual fields (2 had bilateral inferior nasal field loss and 1 had left nasal and right temporal scotomas). Only 1 patient had a lumbar puncture, which yielded an opening pressure of 28 cm H20.
Radiological Features Enhanced CT scans clearly demonstrated the AVMs in all 6 patients. Although the AVMs were also demonstrated on nonenhanced CT, the findings were subtle in 2 patients-1 showed a small area of slightly increased attenuation, and another showed a small, stippled hyperdense lesion (Fig 1). MRI in 5 patients showed areas of decreased signal intensity with irregular serpiginous contours, features that are typical of AVMs. There was no evidence of previous parenchymal hemorrhage on any of the MRI scans. In 1 patient (Patient 6) MRI (after embolization) showed increased signal intensity surrounding the AVM on T2-weighted imaging. This was thought to represent edema secondary to ischemia of the surrounding brain, which correlates with the perfusion defect seen on single photon emission CT. None of the scans showed hydrocephalus suggestive of previous subarachnoid hemorrhage. Moderate mass effect was associated with an AVM in only 1 patient (Patient 5). The lesions were large (nidus greater than 4 cm in diameter) and located in the right parieto-occipital lobes (3 patients), right parietal lobe (2), and left frontal lobe (1 patient). On angiography, the AVMs were supplied by branches of the middle cerebral artery (MCA) and anterior cerebral artery (ACA), with the posterior cerebral artery (PCA) contributing significant branches in 3 patients. All the AVMs drained rapidly into the superior sagittal sinus through large cortical veins. Associated venous obstruction was present in 2 patients (Patients 4 and 6), both of whom had stenosis of the rght transverse sinus at the junction with the sigmoid sinus (Fig 2). Measurements of Cortical Arterial and Venous Pressures Measurements of cortical arterial and venous pressures were obtained in 3 of 4 patients who underwent surgi-
cal excision of the AVMs (Table 2). Normally, cortical artery pressure approaches systemic arterial pressure and cortical venous pressure is 1 to 2 mm Hg above central venous pressure 181. In 2 (Patients 4 and 6) of our 3 patients, the mean cortical feeding artery pressures were substantially less than systemic arterial pressures before AVM excision. The pre-excision cortical draining vein pressures were increased in all 3 patients, and ranged from 16 to 23 mm Hg. After AVM excision the draining vein pressures consistently dropped to 1 to 2 mm Hg above central venous pressures.
Management and Outcome Initial treatment in 3 patients (Patients 2, 3, and 5 ) consisted of medical therapy with acetazolamide, furosemide, and steroids. One patient’s (Patient 2) headaches improved on medical treatment but her visual acuity progressively deteriorated, prompting surgical excision of her AVM 2 months after presentation. The papilledema resolved within 2 months after surgery but there was residual optic atrophy. In another patient (Patient 3) the papilledema persisted unchanged from presentation in 1986 despite treatment with high-dose steroids, acetazolamide, and furosemide, and a course of proton beam irradiation in September 1987. Her acuity and visual fields remain unchanged on a maintenance dose of 250 mg of acetazolamide daily. Because of the size and location of the AVM, the risk of surgery was considered unacceptably high. One patient (Patient 5 ) responded well to dexamethasone, 4 mg four times a day, with resolution of the papilledema within 2 weeks after treatment began. She was maintained for 4 years on acetazolamide, 250 mg three times a day, with no evidence of papilledema, but migrainous headaches with teichopsia persisted. The 3 other patients underwent staged embolization of the AVMs, followed by surgical excision. Papilledema resolved in all 3, with 1 patient showing evidence of postpapilledema optic atrophy l month after surgery. Summary of the Literature Table 1 summarizes the salient clinical and radiological features, as well as outcome, in 6 patients previously reported. The average age was 27 years (range, 11-40 years); 3 were female. Symptoms and signs included papilledema (6 patients), intermittent visual blurring or obscurations (6), headache (4), cranial bruits (2), visual field loss (2), diplopia (l), and pulsatile occipital mass (1 patient). Opening pressures on lumbar puncture in 4 patients ranged from 220 mm H20 to greater than 500 mm H2O. The AVMs were demonstrated on enhanced CT scans in all 5 patients who underwent CT; however, in 3 patients the nonenhanced scans were normal. The patient with the pulsatile right occipital mass had
Chimowia et al: Intracranial Hypertension 475
Table I . Clinical and Radiological Features of Patients with Intracranial Hypertension and Unruptured Cerebral Arteriovenous Malformations (AVMs) Patient Age No. (yr)
Sex Clinical Data
Cleveland Clinic Experience R occipital head1 19 aches since early teens; L hand + face paresthesias; L hemianopic spells; 1 motor seizure involving L hand; papilledema Headaches for 4 wk; 2 21 L ocular TOV when rising from sitting position; progressive bilateral visual loss for 2 wk; papilledema; bilateral inferior field loss
3
32
4
28
5
6
44
24
Literature Cases 7 25 M ~. (Kosary et al. 1973) ~~
Nonenhanced Enhanced AVM CT CT MRI Location
Arterial Supply
Venous Drainage
Other Procedures
R parieto- R MCA, R occipiACA, R tal PCA
sss
-
Opening pres- Developed progressive visual sure of 280 loss on steroids, mm H 2 0 furosemide, and acetazolon LP preamide (visual acuity 201400 treatment OD, 20/80 0 s ) prompting AVM excision 2 mo after initial presentation; papilledema and TOV resolved within 2 mo of surgery; residual bilateral optic atrophy (OD > 0s); 1 yr after surgery, visual acuity 20/400 OD, 20/40 0 s Papilledema persisted 24 mo after presentation despite (1) treatment with prednisone, furosemide, and acetazolamide;(2) proton beam irradiation on 9/87. Fields and acuity remain unchanged
+
+
ND
+
+
+
R parietal
R MCA
sss
Migraine headaches since age 14; several episodes of aphasia, R arm numbness and weakness; L carotid bruit; papilledema; bilateral inferior nasal field loss Generalized seizure 5 yr previously; 3 mo of bifrontal headaches associated with nausea and vomiting; bilateral TOV precipitated by change in posture; Lsided focal motor seizure; R ocular bruit; papilledema R hemicranial headaches since age 12 associated with scintillations in L visual field; intermittent L hand and face numbness; R carotid bruit; papilledema; L nasal and R temporal scotomas 10 spells of L hand numbness and incoordination associated with blurring of L visual field during prior year; 7-hr episode of above symptoms with R frontal headache precipitating admission; papilledema
+
f
+
L frontal
L MCA, L
sss
+
+
+
R occipi- R MCA, R tal-pariPCA, R etal ACA
1% yr of L ocular TOV precipitated by bending over; papilledema
ND
ND
ND
R parietal
ACA
+
+
+
R parietal R MCA, R ACA
+
+
+
R parieto- R MCA, R occipital;
SSS; stenosis of R transverse sinus
Normal preop. SPEC?
sss
-
PCA
maSS
effect displacing R lateral ventricle
476 Annals of Neurology Vol 27 No 5 May 1990
R ACA via the L ACA through the anterior communicating artery
SSS; steR parietal pernosis of fusion defect on R transSPECT verse sinus at junction with sigmoid sinus
sss
-
Treatment and Outcome Embolization followed by AVM excision; LHH following surgery; 2 mo after surgery papilledema resolved, acuity 20/30 bilaterally; partial simple seizure with secondary generalization 1 yr later
Embolization followed by AVM excision; severe.L hemiparesis following surgery; papilledema and TOV resolved within 1 mo of surgery; 4 mo after surgery, mild L hemiparesis and visual acuity and fields n o d
Papilledema resolved within 2 wk of treatment with dexamethasone, acetazolamide, and furosemide; migraine headaches and teichopsia persisted 4 yr later
Embolization followed by AVM resection; LHH following surgery; papilledema resolved within 1 mo of surgery; residual bilateral optic atrophy
Surgical excision of AVM; papilledema decreased from 2-3D to 1D 6 mo after surgery
Table I . (Continued) Patient Age No. (yr)
Nonenhanced
Sex
8 40 M (Weisberg et al. 1977)
9
11
M
(Vassilouthis 1979)
10 31 F (Schiffer et al. 1984)
11 21 F (Barrow 1988)
12 33 F (Barrow 1988)
~~
Clinical Data
a
15 yr of headache ND with worsening over last 4 yr; occasional R ocular T O V pulsatile mass R occiput; R mastoid bruit; papilledema; L inferior homonymous quadrantanopia 5 mo of headache, MUSea, Vomiting; diplopia looking to R; TOV lasting a few seconds; papilledema Sporadic headaches for 10 yr. Worsening of headaches with blurred vision 2 mo before admission; papilledema Headache for several ND years; TOV (R > L) precipitated by moving head; papilledema
1 yr of subjective bruit; bilateral TOV precipitated by change in posw e ; papilledema; peripheral visual loss
Enhanced
Venous Drainage
Other Procedures
Rparieto- RMCA, R occipiACA, R d,R PCA lateral ventricle compressed by AVM
Not specikd
OP = 450
R poste-
R ACA
SSS and ISS
CT
AVM MRI Location
+
ND
+
ND
Arterial Supply
rior frond
-
mm CSF on LP; isotope cistemography showed decreased isotope resorption over cerebral convexities OP = 220 IIUII H 2 0 preop; OP = 120mm H 20 postop
+
ND
Rmidrolandic region
RA CA , R MCA
SSS and internal cerebral vein
+
ND
Rfrontal
RACA
sss
CSF pressure attimeofL Pshunt = 400 mm HzO
i
ND
Lparied lobe
LMCA,L ACA, L PCA
SSS and vein of Galen
OP > 500 IIUII HzO pretreatment; after acetazolamide + furosemide OP > 400 IIUII H 20
~~
Treatment and Outcome OP unchanged after 2 wk of treatment with dexamerhasone; G P shunt resulted in immediate and persistent relief of headache and TOV, papilledema resolved
Surgical excision of AVM, no papilledema 1 yr later
Surgical excision of AVM, L upper extremity paralysis postop resolved over next 4 mo; papilledema not mentioned
Developed early optic atrophy on dexamethasone and acetazolamide, prompting L P shunt; papilledema worsened despite functioning shunt; surgical excision of AVM resulted in resolution of papilledema 2 mo after operation Developed peripheral visual loss on acetazolamide and furosemide; surgical excision resulted in resolution of papilledema within 3 mo of surgery; developed cerebral edema 36 hr after surgery from which she recovered !idly
~~
D = diopter; ND = not done or reported; MCA = middle cerebral artery; ACA = antenor cerebral artery, PCA = posterior cerebral artery; SSS = superior s a g i d sinus; ISS = inferior s a g r d sinus; OP = opemng pressure; LF' = lumbar puncture; L P = lumbar-peritoneal; LHH = left homonymous hemianopia; SPECT = single photon emission computed tomography; OD = right eye; 0 s = left eye; TOV = transient obscurations of vision.
sgdicant mass effect, with obliteration of the body and atrium of the right lateral ventricle. All the AVMs were supplied by the ACA, with the MCA contributing in 3 patients and the PCA in 2 patients. The venous drainage was into the superior sagittal sinus in 5 patients, and not specified in the other. Isotope cisternography in 1 patient (Patient 8) showed decreased absorption of isotope over the cerebral convexities bilaterally, more so on the right. Three patients underwent surgical excision of the AVMs, with resolution of papilledema. In 3 other patients pharmacological therapy initially failed to lower intracranial pressure. One had persistently raised intracranial pressure prompting insertion of a lumbarperitoneal shunt, which successfully reversed the papilledema. Another developed optic atrophy prompting insertion of a lumbar-peritoneal shunt, which resulted in temporary improvement in headache and papilledema, but 3 months later the papilledema worsened
despite a functioning shunt. She underwent surgical excision of the AVM, with resolution of the visual obscurations and papilledema 2 months after surgery. The last patient underwent surgical excision of the AVM because she had progressive peripheral visual loss when treated with acetazolamide, furosemide, and prednisone. Measurements of arterial and venous pressures during surgery showed a feeding artery pressure of 35 mm Hg before excision, with a systemic arterial pressure of 7 1 mm Hg. After excision of the AVM the feeding artery pressure rose to 75 mm Hg. The draining vein pressure was 20 mm Hg before excision when the central venous pressure was 9 mm Hg.
Discussion Although intracranial hypertension is well recognized as a presentation of dural AVMs [lo-131, it is an uncommon feature of cerebral AVMs. The incidence of intracranial hypertension associated with unrupChimowitz et al: Intracranial Hypertension
477
Fig I . Radiologicalfindings in Patient 2. (A)Nonenhanced C T , initially interpreted as normal, demonstrates a small, stippled, hyperdense lesion which probably represents calcification of part of the arteriovenous malforrnution. (B) Enhanced CT clearly demonstrates right parietal arteriovenous malformation. (C) Angiogram showing large right parietal arteriovenous malformation supplied by the right middle cerebral artery and draining into large cortical veins.
tured cerebral AVMs is unknown, but our experience with only 6 patients in the last 10 years and the paucity of reports in the literature suggest that it is rare. Our 6 patients share certain common features with the 6 patients previously reported. All were young patients with high flow AVMs draining primarily into the superior sagittal sinus. Typically these patients presented with headache, visual obscurations, and papilledema, suggesting a cerebral mass lesion or pseudotumor cerebri. An important clinical sign suggesting a cerebral AVM was a cranial or ocular bruit in 5 of 12 patients. In 4 patients (Patients 2, 9, 10, 12) nonenhanced CT scans were reported as normal. In 1 patient (Patient 12) this led to an erroneous initial diagnosis of pseudotumor cerebri which was discovered only at a later date when medical treatment failed and an enhanced CT scan showed an AVM. These cases emphasize the importance of obtaining an enhanced CT scan or MRI in patients with suspected pseudotumor cerebri. Pharmacological therapy was ineffective in controlling the intracranial hypertension in 5 of 6 patients, and 3 patients developed progressive visual loss during medical therapy. In contrast, excision of the AVM effectively reduced intracranial hypertension in all 9 patients who ultimately underwent surgery. These results suggest that surgical excision of the AVM, if it can be done with low risk, is the treatment of choice to lower intracranial hypertension in patients with unruptured cerebral AVMs. Alternative therapeutic options include lumbar-peritoneal shunting, which may effectively reduce the intracranial hypertension in this setting, or optic nerve sheath decompression to relieve 478 Annals of Neurology Vol 27 No 5 May 1990
Fig 2. Venousphase ofthe angiogram of Patient 6 demonstrating drainage of the arteriovenous malformation into the superior sagittal sinus and stenosis of the right transverse sinus at the junction with the sigmoid sinus (arrow).
chronic papilledema { 14, 15}. However, these young patients are at substantial long-term risk of cerebral hemorrhage 1161 and probably warrant removal of the AVM on this basis alone. There are several possible mechanisms of intracranial hypertension with an unruptured cerebral AVM. In 2 patients (Patient 5 and S), the AVMs acted as mass lesions producing effacement and shift of the ventricular system. In the other 10 patients the intracranial hypertension was likely related to the hemodynamic characteristics of AVMs. The intraoperative pressure measurements in 4 patients (Patients 2, 4, 6, and 12) consistently showed substantial reduction in feeding artery pressures and substantial elevation in draining vein pressures. Transmission of high pressures to the venous side of the shunt likely increased the superior sagittal sinus pressure since this was the major drainage pathway for all of these AVMs. Although we did not measure superior saggital sinus pressure to confirm this, Lamas and colleagues 117)
Table 2. Measurements of Arterial and Venous Pressures (mm Hg) before Remwal of Arteriwenous Malformation Mean Arterial Pressure
Mean Venous Pressure
Patient No.
FAP"
SAP
DVP
CVP
2
70 37 20
70
21 16 23
10
75 74
4 6
"Normal cortical artery pressure = (0.90-1.00) pressure [S].
X
7 3 systemic arterial
FAP = feeding artery pressure; SAP = systemic arterial blood pressure; DVP = draining vein pressure; CVP = central venous pressure.
catheterized the superior sagittal sinus in a patient with papilledema and a posterior fossa dural AVM and found that superior sagittal sinus pressures were consistently elevated to values 2 to 3 mm Hg lower than intracranial pressure. Elevated superior sagittal sinus pressure may produce intracranial hypertension by increasing cerebral blood volume, secondary to vasodilation caused by decreased cerebral perfusion pressure, and by impairing cerebrospinal fluid (CSF) absorption. Evidence for the latter mechanism is provided by 1 patient (Patient 8) whose isotope cisternography showed delayed resorption of CSF, prompting insertion of a lumbar-peritoneal shunt, which resulted in resolution of the patient's papilledema. However, failure of lumbar-peritoneal shunting in 1 patient (Patient 11) suggests that factors in addition to decreased CSF absorption (i.e., increased cerebral blood volume) are important in the genesis of intracranial hypertension in this setting. It is uncertain why only rare patients with high-flow cerebral AVMs that drain into the superior sagittal sinus develop raised intracranial pressure, since this is a common angiographic pattern. One possibility may be that these patients have pseudotumor cerebri accounting for intracranial hypertension and an incidental ,AVM. However, the equal incidence among males and females, the failure of medical therapy to control the raised intracranial pressure, and the resolution of papilledema after excision of the AVM argue strongly against this thesis. Another more plausible explanation is that venous hypertension in association with cerebral AVMs requires not only increased blood flow through the AVM shunt, but also partial obstruction of venous outflow. Evidence for this theory is provided by 2 patients (Patients 4 and 6), both of whom had stenosis of the right transverse sinus at its junction with the sigmoid sinus (see Fig 2). Zabramski and Spetzler 1181 provided additional supporting evidence for this theory in && brief description of a child with an UnruP-
tured AVM and symptoms of venous hypertension in whom venous outflow obstruction seemed to be caused by congenitally small jugular bulbs bilaterally. Unfortunately, the venous phase studies in the majority of our patients and the angiographic images provided in the literature were inadequate to assess venous outflow obstruction beyond the superior sagittal sinus. Detailed study of venous outflow in patients with unruptured cerebral AVMs and raised intracranial pressure will determine whether venous obstruction is a necessary condition for the development of intracranial hypertension.
References 1. Paterson JH, McKissock W. A clinical survey of intracranial angiomas with special reference to their mode of progression and surgical treatment: a report of 110 cases. Brain 1955; 79233-266 2. Kosary 12, Treister G, Tadmor R. Transient monocular amaurosis due to a contralateral cerebral vascular malformation. Neurochirurgia 1973;16:127-1 30 3. Weisberg LA, Pierce JF, Jabbari B. Intracranial hypertension resulting from a cerebrovascular malformation. South Med J 1977;70624-626 4. Vassilouthis J. Cerebral arteriovenous malformation with intracranial hypertension. Surg Neurol 1979;11:402-404 5. Schiffer J,-Bibi C, Avida D. Cerebral arteriovenous malformation: papilledema as a presenting sign. Surg Neurol 1984; 22~524-526 6. Barrow DL. Unmptured cerebral arteriovenous malformations presenting with intracranial hypertension. Neurosurgery 1988; 23:484-490 7. Barnett GH, Little JR, Ebrahim ZY, et al. Cerebral circulation during arteriovenous malformation operation. Neurosurgery 1987;20:836-842 8. Little JR, Tomsak RL, Ebrahim Z Y , Furlan AJ. Retinal artery pressure and cerebral artery perfusion pressure in cerebrovascular occlusive disease. Neurosurgery 1986;18:716-720 9. Leblanc R, Little JR. Hemodynamics of arteriovenous malformations. Clin Neurosurg 1989;36:299-317 10. Houser OW, Campbell JK, Campbell RJ, Sundt TM. Arteriovenous malformation affecting the transverse dural venous sinusan acquired lesion. Mayo Clin Proc 1979;54:651-661 11. Gelwan MJ, Choi IS, Berenstein A, et al. Dural arteriovenous malformations and papilledema. Neurosurgery 1988;22:10791084 12. Kuhner A, Krastel A, Stoll W. Arteriovenous malformations of the transverse dural sinus. J Neurosurg 1976;45:12-19 13. Nicola GC, Nizzoli V. Dural arteriovenous malformations of the posterior fossa J Neurol Neurosurg Psychiatry 1968;31: 514-519 14. Burde RM, Karp JS, Miller RN. Reversal of visual deficit with optic nerve decompression in long-standing pseudotumor cerebri. Am J Ophthalmol 1974;77:770-772 1 5 . Billson FA, Hudson RL. Surgical treatment of chronic papilloedema in children. Br J Ophthalmol 1975;59:92-95 16. Brown RD Jr, Wiebers DO, Forbes G, et al. The natural history of unruptured intracranial arteriovenous malformations.J Neurosurg 1988;68:352-357 17. Lamas E, Lobato RD, Espana J, Escudero L. Dural posterior fossa AVM producing raised sagittal sinus pressure. J Neurosurg 1977;46:804-810 18. Zabramski JM, Spealer RF. AVMs and intracranial hypertension (Comments). Neurosurgery 1988;23:489
Chimowitz et al: Intracranial Hypertension 479
Only 6 patients with intracranial hypertension associated with unruptured cerebral arteriovenous malformations have been reported. We report 6 additional patients seen at the Cleveland Clinic during the past 10 years. The average age was 28 years (range, 19-44 years); 4 were women. Symptoms and signs included papilledema (6patients), headache (6), transient nonepileptic focal symptoms (4),visual obscurations (3,ipsilateral carotid or ocular bruits (3), abnormal visual fields (3), focal seizures (2), and progressive visual loss (1). Enhanced computed tomography (CT) or magnetic resonance imaging (MRI) demonstrated the malformations in all 6 patients. The malformations were large, supplied by the branches of the middle and anterior cerebral arteries, with the posterior cerebral artery contributing in 3 patients, and all drained into the superior sagittal sinus. Associated venous obstruction was seen in 2 patients. Four patients underwent excision of the arteriovenous malformation, with resolution of papilledema in all 4. Measurements of cortical arterial and venous pressures during surgery in 3 patients showed decreased feeding artery pressures and elevated draining vein pressures, which normalized after removal of the malformation. Treatment in the 2 remaining patients consisted of medical therapy (acetazolamide, furosemide, steroids) alone in 1 patient, and in conjunction with proton beam radiation in the other. Papilledema resolved in the former patient, but the patient receiving proton beam radiation still had papilledema 2 years later. Intracranial hypertension associated with unruptured cerebral arteriovenous malformations occurs in young patients with high flow malformations that drain into the superior sagittal sinus, and is likely the result of increased cortical venous and superior sagittal sinus pressure. Excision of the malformation effectively reduces the intracranial pressure. Chimowitz MI, Little JR, Awad IA, Sila CA, Kosmorsky G, Furlan AJ. Intracranial hypertension associated with unruptured cerebral arteriovenous malformations. Ann Neurol 1990;27:474-479
Intracranial hypertension is an uncommon presenta-
tion of unruptured cerebral arteriovenous malformations (AVMs). In a clinical survey of 110 intracranial angiomas reported in 1955, Paterson and McKissock briefly described 1 patient with an unruptured occipital angioma and papilledema [l). Since then only 6 patients have been reported [2-61. We report 6 additional patients with unruptured cerebral AVMs and intracranial hypertension; review the literature; and attempt to clarify the clinical, radiological, and pathophysiological features of this unusual entity.
Methods The 6 patients represent a nonconsecutive, selected group identified over a 10-year period (1979-1989) at the Cleveland Clinic. Evaluation of each patient included a neurological assessment by at least one of us, neuro-ophthalmological consultation with formal visual fields, cranial computed tomography (CT) or magnetic resonance imaging (MRI), and From the Departments of *Neurology, ?Neurosurgery, and SNeuroOphthalmology, Cleveland Clinic Foundation, Cleveland, OH. Received Jun 23, 1989, and in revised form Oct 27. Accepted for publication Oct 27, 1989.
three-vessel cerebral angiography. Four patients underwent complete microsurgical removal of the AVMs. These procedures were carried out under general anesthesia with the patient positioned supine. After dural opening, measurements of cortical arterial and venous pressures were carried out in 3 of the 4 patients. This technique was previously described in detail 17-31. A 26-gauge needle was coupled to a strain gauge transducer by semirigid fluid-filled tubing. All pressure transducers, including the one measuring the systemic arterial blood pressure, were leveled to the right atrium of the heart. The feeding artery pressure was measured before excision of the AVM by inserting the needle under microscopic visualization into a segment of the artery within 1 cm of the AVM margin. Draining vein pressure was then measured by inserting the needle into a major vein draining arteridzed blood within 1 cm of the AVM margin. Measurement of draining vein pressure was repeated after AVM excision. Outcome in all patients was closely monitored over periods ranging from 4 months to 10 years since initial diagnosis. An extensive review of the English literature yielded 6 Address correspondence to Dr Furlan, Department of Neurology, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195.
474 Copyright 0 1990 by the American Neurological Association
previously reported patients with unruptured cerebral AVMs and intracranial hypertension 12-61. Results Clinical Features Table 1 summarizes the clinical and radiological findings and outcome in our 6 patients. The average age of the 6 patients was 28 years (range, 19-44 years); 4 were women. Presenting symptoms included headache (6 patients); transient language, motor, or sensory symptoms (4); visual obscurations (3); focal seizures (2); and progressive bilateral visual loss (1). Signs included papilledema (6 patients), ipsilateral carotid or ocular bruits (3), and abnormal visual fields (2 had bilateral inferior nasal field loss and 1 had left nasal and right temporal scotomas). Only 1 patient had a lumbar puncture, which yielded an opening pressure of 28 cm H20.
Radiological Features Enhanced CT scans clearly demonstrated the AVMs in all 6 patients. Although the AVMs were also demonstrated on nonenhanced CT, the findings were subtle in 2 patients-1 showed a small area of slightly increased attenuation, and another showed a small, stippled hyperdense lesion (Fig 1). MRI in 5 patients showed areas of decreased signal intensity with irregular serpiginous contours, features that are typical of AVMs. There was no evidence of previous parenchymal hemorrhage on any of the MRI scans. In 1 patient (Patient 6) MRI (after embolization) showed increased signal intensity surrounding the AVM on T2-weighted imaging. This was thought to represent edema secondary to ischemia of the surrounding brain, which correlates with the perfusion defect seen on single photon emission CT. None of the scans showed hydrocephalus suggestive of previous subarachnoid hemorrhage. Moderate mass effect was associated with an AVM in only 1 patient (Patient 5). The lesions were large (nidus greater than 4 cm in diameter) and located in the right parieto-occipital lobes (3 patients), right parietal lobe (2), and left frontal lobe (1 patient). On angiography, the AVMs were supplied by branches of the middle cerebral artery (MCA) and anterior cerebral artery (ACA), with the posterior cerebral artery (PCA) contributing significant branches in 3 patients. All the AVMs drained rapidly into the superior sagittal sinus through large cortical veins. Associated venous obstruction was present in 2 patients (Patients 4 and 6), both of whom had stenosis of the rght transverse sinus at the junction with the sigmoid sinus (Fig 2). Measurements of Cortical Arterial and Venous Pressures Measurements of cortical arterial and venous pressures were obtained in 3 of 4 patients who underwent surgi-
cal excision of the AVMs (Table 2). Normally, cortical artery pressure approaches systemic arterial pressure and cortical venous pressure is 1 to 2 mm Hg above central venous pressure 181. In 2 (Patients 4 and 6) of our 3 patients, the mean cortical feeding artery pressures were substantially less than systemic arterial pressures before AVM excision. The pre-excision cortical draining vein pressures were increased in all 3 patients, and ranged from 16 to 23 mm Hg. After AVM excision the draining vein pressures consistently dropped to 1 to 2 mm Hg above central venous pressures.
Management and Outcome Initial treatment in 3 patients (Patients 2, 3, and 5 ) consisted of medical therapy with acetazolamide, furosemide, and steroids. One patient’s (Patient 2) headaches improved on medical treatment but her visual acuity progressively deteriorated, prompting surgical excision of her AVM 2 months after presentation. The papilledema resolved within 2 months after surgery but there was residual optic atrophy. In another patient (Patient 3) the papilledema persisted unchanged from presentation in 1986 despite treatment with high-dose steroids, acetazolamide, and furosemide, and a course of proton beam irradiation in September 1987. Her acuity and visual fields remain unchanged on a maintenance dose of 250 mg of acetazolamide daily. Because of the size and location of the AVM, the risk of surgery was considered unacceptably high. One patient (Patient 5 ) responded well to dexamethasone, 4 mg four times a day, with resolution of the papilledema within 2 weeks after treatment began. She was maintained for 4 years on acetazolamide, 250 mg three times a day, with no evidence of papilledema, but migrainous headaches with teichopsia persisted. The 3 other patients underwent staged embolization of the AVMs, followed by surgical excision. Papilledema resolved in all 3, with 1 patient showing evidence of postpapilledema optic atrophy l month after surgery. Summary of the Literature Table 1 summarizes the salient clinical and radiological features, as well as outcome, in 6 patients previously reported. The average age was 27 years (range, 11-40 years); 3 were female. Symptoms and signs included papilledema (6 patients), intermittent visual blurring or obscurations (6), headache (4), cranial bruits (2), visual field loss (2), diplopia (l), and pulsatile occipital mass (1 patient). Opening pressures on lumbar puncture in 4 patients ranged from 220 mm H20 to greater than 500 mm H2O. The AVMs were demonstrated on enhanced CT scans in all 5 patients who underwent CT; however, in 3 patients the nonenhanced scans were normal. The patient with the pulsatile right occipital mass had
Chimowia et al: Intracranial Hypertension 475
Table I . Clinical and Radiological Features of Patients with Intracranial Hypertension and Unruptured Cerebral Arteriovenous Malformations (AVMs) Patient Age No. (yr)
Sex Clinical Data
Cleveland Clinic Experience R occipital head1 19 aches since early teens; L hand + face paresthesias; L hemianopic spells; 1 motor seizure involving L hand; papilledema Headaches for 4 wk; 2 21 L ocular TOV when rising from sitting position; progressive bilateral visual loss for 2 wk; papilledema; bilateral inferior field loss
3
32
4
28
5
6
44
24
Literature Cases 7 25 M ~. (Kosary et al. 1973) ~~
Nonenhanced Enhanced AVM CT CT MRI Location
Arterial Supply
Venous Drainage
Other Procedures
R parieto- R MCA, R occipiACA, R tal PCA
sss
-
Opening pres- Developed progressive visual sure of 280 loss on steroids, mm H 2 0 furosemide, and acetazolon LP preamide (visual acuity 201400 treatment OD, 20/80 0 s ) prompting AVM excision 2 mo after initial presentation; papilledema and TOV resolved within 2 mo of surgery; residual bilateral optic atrophy (OD > 0s); 1 yr after surgery, visual acuity 20/400 OD, 20/40 0 s Papilledema persisted 24 mo after presentation despite (1) treatment with prednisone, furosemide, and acetazolamide;(2) proton beam irradiation on 9/87. Fields and acuity remain unchanged
+
+
ND
+
+
+
R parietal
R MCA
sss
Migraine headaches since age 14; several episodes of aphasia, R arm numbness and weakness; L carotid bruit; papilledema; bilateral inferior nasal field loss Generalized seizure 5 yr previously; 3 mo of bifrontal headaches associated with nausea and vomiting; bilateral TOV precipitated by change in posture; Lsided focal motor seizure; R ocular bruit; papilledema R hemicranial headaches since age 12 associated with scintillations in L visual field; intermittent L hand and face numbness; R carotid bruit; papilledema; L nasal and R temporal scotomas 10 spells of L hand numbness and incoordination associated with blurring of L visual field during prior year; 7-hr episode of above symptoms with R frontal headache precipitating admission; papilledema
+
f
+
L frontal
L MCA, L
sss
+
+
+
R occipi- R MCA, R tal-pariPCA, R etal ACA
1% yr of L ocular TOV precipitated by bending over; papilledema
ND
ND
ND
R parietal
ACA
+
+
+
R parietal R MCA, R ACA
+
+
+
R parieto- R MCA, R occipital;
SSS; stenosis of R transverse sinus
Normal preop. SPEC?
sss
-
PCA
maSS
effect displacing R lateral ventricle
476 Annals of Neurology Vol 27 No 5 May 1990
R ACA via the L ACA through the anterior communicating artery
SSS; steR parietal pernosis of fusion defect on R transSPECT verse sinus at junction with sigmoid sinus
sss
-
Treatment and Outcome Embolization followed by AVM excision; LHH following surgery; 2 mo after surgery papilledema resolved, acuity 20/30 bilaterally; partial simple seizure with secondary generalization 1 yr later
Embolization followed by AVM excision; severe.L hemiparesis following surgery; papilledema and TOV resolved within 1 mo of surgery; 4 mo after surgery, mild L hemiparesis and visual acuity and fields n o d
Papilledema resolved within 2 wk of treatment with dexamethasone, acetazolamide, and furosemide; migraine headaches and teichopsia persisted 4 yr later
Embolization followed by AVM resection; LHH following surgery; papilledema resolved within 1 mo of surgery; residual bilateral optic atrophy
Surgical excision of AVM; papilledema decreased from 2-3D to 1D 6 mo after surgery
Table I . (Continued) Patient Age No. (yr)
Nonenhanced
Sex
8 40 M (Weisberg et al. 1977)
9
11
M
(Vassilouthis 1979)
10 31 F (Schiffer et al. 1984)
11 21 F (Barrow 1988)
12 33 F (Barrow 1988)
~~
Clinical Data
a
15 yr of headache ND with worsening over last 4 yr; occasional R ocular T O V pulsatile mass R occiput; R mastoid bruit; papilledema; L inferior homonymous quadrantanopia 5 mo of headache, MUSea, Vomiting; diplopia looking to R; TOV lasting a few seconds; papilledema Sporadic headaches for 10 yr. Worsening of headaches with blurred vision 2 mo before admission; papilledema Headache for several ND years; TOV (R > L) precipitated by moving head; papilledema
1 yr of subjective bruit; bilateral TOV precipitated by change in posw e ; papilledema; peripheral visual loss
Enhanced
Venous Drainage
Other Procedures
Rparieto- RMCA, R occipiACA, R d,R PCA lateral ventricle compressed by AVM
Not specikd
OP = 450
R poste-
R ACA
SSS and ISS
CT
AVM MRI Location
+
ND
+
ND
Arterial Supply
rior frond
-
mm CSF on LP; isotope cistemography showed decreased isotope resorption over cerebral convexities OP = 220 IIUII H 2 0 preop; OP = 120mm H 20 postop
+
ND
Rmidrolandic region
RA CA , R MCA
SSS and internal cerebral vein
+
ND
Rfrontal
RACA
sss
CSF pressure attimeofL Pshunt = 400 mm HzO
i
ND
Lparied lobe
LMCA,L ACA, L PCA
SSS and vein of Galen
OP > 500 IIUII HzO pretreatment; after acetazolamide + furosemide OP > 400 IIUII H 20
~~
Treatment and Outcome OP unchanged after 2 wk of treatment with dexamerhasone; G P shunt resulted in immediate and persistent relief of headache and TOV, papilledema resolved
Surgical excision of AVM, no papilledema 1 yr later
Surgical excision of AVM, L upper extremity paralysis postop resolved over next 4 mo; papilledema not mentioned
Developed early optic atrophy on dexamethasone and acetazolamide, prompting L P shunt; papilledema worsened despite functioning shunt; surgical excision of AVM resulted in resolution of papilledema 2 mo after operation Developed peripheral visual loss on acetazolamide and furosemide; surgical excision resulted in resolution of papilledema within 3 mo of surgery; developed cerebral edema 36 hr after surgery from which she recovered !idly
~~
D = diopter; ND = not done or reported; MCA = middle cerebral artery; ACA = antenor cerebral artery, PCA = posterior cerebral artery; SSS = superior s a g i d sinus; ISS = inferior s a g r d sinus; OP = opemng pressure; LF' = lumbar puncture; L P = lumbar-peritoneal; LHH = left homonymous hemianopia; SPECT = single photon emission computed tomography; OD = right eye; 0 s = left eye; TOV = transient obscurations of vision.
sgdicant mass effect, with obliteration of the body and atrium of the right lateral ventricle. All the AVMs were supplied by the ACA, with the MCA contributing in 3 patients and the PCA in 2 patients. The venous drainage was into the superior sagittal sinus in 5 patients, and not specified in the other. Isotope cisternography in 1 patient (Patient 8) showed decreased absorption of isotope over the cerebral convexities bilaterally, more so on the right. Three patients underwent surgical excision of the AVMs, with resolution of papilledema. In 3 other patients pharmacological therapy initially failed to lower intracranial pressure. One had persistently raised intracranial pressure prompting insertion of a lumbarperitoneal shunt, which successfully reversed the papilledema. Another developed optic atrophy prompting insertion of a lumbar-peritoneal shunt, which resulted in temporary improvement in headache and papilledema, but 3 months later the papilledema worsened
despite a functioning shunt. She underwent surgical excision of the AVM, with resolution of the visual obscurations and papilledema 2 months after surgery. The last patient underwent surgical excision of the AVM because she had progressive peripheral visual loss when treated with acetazolamide, furosemide, and prednisone. Measurements of arterial and venous pressures during surgery showed a feeding artery pressure of 35 mm Hg before excision, with a systemic arterial pressure of 7 1 mm Hg. After excision of the AVM the feeding artery pressure rose to 75 mm Hg. The draining vein pressure was 20 mm Hg before excision when the central venous pressure was 9 mm Hg.
Discussion Although intracranial hypertension is well recognized as a presentation of dural AVMs [lo-131, it is an uncommon feature of cerebral AVMs. The incidence of intracranial hypertension associated with unrupChimowitz et al: Intracranial Hypertension
477
Fig I . Radiologicalfindings in Patient 2. (A)Nonenhanced C T , initially interpreted as normal, demonstrates a small, stippled, hyperdense lesion which probably represents calcification of part of the arteriovenous malforrnution. (B) Enhanced CT clearly demonstrates right parietal arteriovenous malformation. (C) Angiogram showing large right parietal arteriovenous malformation supplied by the right middle cerebral artery and draining into large cortical veins.
tured cerebral AVMs is unknown, but our experience with only 6 patients in the last 10 years and the paucity of reports in the literature suggest that it is rare. Our 6 patients share certain common features with the 6 patients previously reported. All were young patients with high flow AVMs draining primarily into the superior sagittal sinus. Typically these patients presented with headache, visual obscurations, and papilledema, suggesting a cerebral mass lesion or pseudotumor cerebri. An important clinical sign suggesting a cerebral AVM was a cranial or ocular bruit in 5 of 12 patients. In 4 patients (Patients 2, 9, 10, 12) nonenhanced CT scans were reported as normal. In 1 patient (Patient 12) this led to an erroneous initial diagnosis of pseudotumor cerebri which was discovered only at a later date when medical treatment failed and an enhanced CT scan showed an AVM. These cases emphasize the importance of obtaining an enhanced CT scan or MRI in patients with suspected pseudotumor cerebri. Pharmacological therapy was ineffective in controlling the intracranial hypertension in 5 of 6 patients, and 3 patients developed progressive visual loss during medical therapy. In contrast, excision of the AVM effectively reduced intracranial hypertension in all 9 patients who ultimately underwent surgery. These results suggest that surgical excision of the AVM, if it can be done with low risk, is the treatment of choice to lower intracranial hypertension in patients with unruptured cerebral AVMs. Alternative therapeutic options include lumbar-peritoneal shunting, which may effectively reduce the intracranial hypertension in this setting, or optic nerve sheath decompression to relieve 478 Annals of Neurology Vol 27 No 5 May 1990
Fig 2. Venousphase ofthe angiogram of Patient 6 demonstrating drainage of the arteriovenous malformation into the superior sagittal sinus and stenosis of the right transverse sinus at the junction with the sigmoid sinus (arrow).
chronic papilledema { 14, 15}. However, these young patients are at substantial long-term risk of cerebral hemorrhage 1161 and probably warrant removal of the AVM on this basis alone. There are several possible mechanisms of intracranial hypertension with an unruptured cerebral AVM. In 2 patients (Patient 5 and S), the AVMs acted as mass lesions producing effacement and shift of the ventricular system. In the other 10 patients the intracranial hypertension was likely related to the hemodynamic characteristics of AVMs. The intraoperative pressure measurements in 4 patients (Patients 2, 4, 6, and 12) consistently showed substantial reduction in feeding artery pressures and substantial elevation in draining vein pressures. Transmission of high pressures to the venous side of the shunt likely increased the superior sagittal sinus pressure since this was the major drainage pathway for all of these AVMs. Although we did not measure superior saggital sinus pressure to confirm this, Lamas and colleagues 117)
Table 2. Measurements of Arterial and Venous Pressures (mm Hg) before Remwal of Arteriwenous Malformation Mean Arterial Pressure
Mean Venous Pressure
Patient No.
FAP"
SAP
DVP
CVP
2
70 37 20
70
21 16 23
10
75 74
4 6
"Normal cortical artery pressure = (0.90-1.00) pressure [S].
X
7 3 systemic arterial
FAP = feeding artery pressure; SAP = systemic arterial blood pressure; DVP = draining vein pressure; CVP = central venous pressure.
catheterized the superior sagittal sinus in a patient with papilledema and a posterior fossa dural AVM and found that superior sagittal sinus pressures were consistently elevated to values 2 to 3 mm Hg lower than intracranial pressure. Elevated superior sagittal sinus pressure may produce intracranial hypertension by increasing cerebral blood volume, secondary to vasodilation caused by decreased cerebral perfusion pressure, and by impairing cerebrospinal fluid (CSF) absorption. Evidence for the latter mechanism is provided by 1 patient (Patient 8) whose isotope cisternography showed delayed resorption of CSF, prompting insertion of a lumbar-peritoneal shunt, which resulted in resolution of the patient's papilledema. However, failure of lumbar-peritoneal shunting in 1 patient (Patient 11) suggests that factors in addition to decreased CSF absorption (i.e., increased cerebral blood volume) are important in the genesis of intracranial hypertension in this setting. It is uncertain why only rare patients with high-flow cerebral AVMs that drain into the superior sagittal sinus develop raised intracranial pressure, since this is a common angiographic pattern. One possibility may be that these patients have pseudotumor cerebri accounting for intracranial hypertension and an incidental ,AVM. However, the equal incidence among males and females, the failure of medical therapy to control the raised intracranial pressure, and the resolution of papilledema after excision of the AVM argue strongly against this thesis. Another more plausible explanation is that venous hypertension in association with cerebral AVMs requires not only increased blood flow through the AVM shunt, but also partial obstruction of venous outflow. Evidence for this theory is provided by 2 patients (Patients 4 and 6), both of whom had stenosis of the right transverse sinus at its junction with the sigmoid sinus (see Fig 2). Zabramski and Spetzler 1181 provided additional supporting evidence for this theory in && brief description of a child with an UnruP-
tured AVM and symptoms of venous hypertension in whom venous outflow obstruction seemed to be caused by congenitally small jugular bulbs bilaterally. Unfortunately, the venous phase studies in the majority of our patients and the angiographic images provided in the literature were inadequate to assess venous outflow obstruction beyond the superior sagittal sinus. Detailed study of venous outflow in patients with unruptured cerebral AVMs and raised intracranial pressure will determine whether venous obstruction is a necessary condition for the development of intracranial hypertension.
References 1. Paterson JH, McKissock W. A clinical survey of intracranial angiomas with special reference to their mode of progression and surgical treatment: a report of 110 cases. Brain 1955; 79233-266 2. Kosary 12, Treister G, Tadmor R. Transient monocular amaurosis due to a contralateral cerebral vascular malformation. Neurochirurgia 1973;16:127-1 30 3. Weisberg LA, Pierce JF, Jabbari B. Intracranial hypertension resulting from a cerebrovascular malformation. South Med J 1977;70624-626 4. Vassilouthis J. Cerebral arteriovenous malformation with intracranial hypertension. Surg Neurol 1979;11:402-404 5. Schiffer J,-Bibi C, Avida D. Cerebral arteriovenous malformation: papilledema as a presenting sign. Surg Neurol 1984; 22~524-526 6. Barrow DL. Unmptured cerebral arteriovenous malformations presenting with intracranial hypertension. Neurosurgery 1988; 23:484-490 7. Barnett GH, Little JR, Ebrahim ZY, et al. Cerebral circulation during arteriovenous malformation operation. Neurosurgery 1987;20:836-842 8. Little JR, Tomsak RL, Ebrahim Z Y , Furlan AJ. Retinal artery pressure and cerebral artery perfusion pressure in cerebrovascular occlusive disease. Neurosurgery 1986;18:716-720 9. Leblanc R, Little JR. Hemodynamics of arteriovenous malformations. Clin Neurosurg 1989;36:299-317 10. Houser OW, Campbell JK, Campbell RJ, Sundt TM. Arteriovenous malformation affecting the transverse dural venous sinusan acquired lesion. Mayo Clin Proc 1979;54:651-661 11. Gelwan MJ, Choi IS, Berenstein A, et al. Dural arteriovenous malformations and papilledema. Neurosurgery 1988;22:10791084 12. Kuhner A, Krastel A, Stoll W. Arteriovenous malformations of the transverse dural sinus. J Neurosurg 1976;45:12-19 13. Nicola GC, Nizzoli V. Dural arteriovenous malformations of the posterior fossa J Neurol Neurosurg Psychiatry 1968;31: 514-519 14. Burde RM, Karp JS, Miller RN. Reversal of visual deficit with optic nerve decompression in long-standing pseudotumor cerebri. Am J Ophthalmol 1974;77:770-772 1 5 . Billson FA, Hudson RL. Surgical treatment of chronic papilloedema in children. Br J Ophthalmol 1975;59:92-95 16. Brown RD Jr, Wiebers DO, Forbes G, et al. The natural history of unruptured intracranial arteriovenous malformations.J Neurosurg 1988;68:352-357 17. Lamas E, Lobato RD, Espana J, Escudero L. Dural posterior fossa AVM producing raised sagittal sinus pressure. J Neurosurg 1977;46:804-810 18. Zabramski JM, Spealer RF. AVMs and intracranial hypertension (Comments). Neurosurgery 1988;23:489
Chimowitz et al: Intracranial Hypertension 479
