Intracranial hypertension and papilledema secondary to an unruptured arteriovenous malformation: Review of the literature

Abstract

Arteriovenous malformations (AVMs) are abnormal connections of arteries and veins without intermediate capillary components. As such, AVMs can remain asymptomatic or have a variety of clinical presentations ranging from mild headaches to severe symptoms like seizures, hemorrhage, and subsequent coma. Papilledema and increased intracranial pressure without hydrocephalus or hemorrhage are rare forms of presentations of cerebral AVM. The mechanism of intracranial hypertension accompanying brain AVMs is not entirely understood, and the right treatment strategy is controversial. Here, we present the treatment and outcomes of four patients with unruptured AVMs who presented with intracranial hypertension accompanied by visual symptoms, papilledema, and without evidence of hydrocephalus. In cases of AVMs accompanied by intracranial hypertension, AVM treatment should be considered the main target of management.

Introduction

Although frequently asymptomatic, arteriovenous malformations (AVMs) may present with a broad variety of symptoms ranging from nonspecific headaches to intracerebral hemorrhage resulting in severe neurologic deficits. ¹ Increased intracranial pressure, as a result of hemorrhage and hydrocephalus, is a common presentation of such malformations. However, clinical manifestation with papilledema in the absence of cerebral hemorrhage and hydrocephalus, similar to benign intracranial hypertension, is very rare. No definitive etiology has ever been reported for this kind of presentation and the suggested treatment strategies include medical therapy, CSF diversion shunts, or endovascular embolization and/or surgical resection of the lesion.^1–3 In this article, we present four patients with visual presentations and symptoms of increased intracranial pressure who underwent endovascular treatment and provide a literature review of previous case.

Case series

Case 1

A 35-year-old male presented with intermittent headaches and blurred vision. On ophthalmologic examination, he had bilateral Papilledema. Computed Tomography (CT) ⁴ and Magnetic Resonance Imaging (MRI) revealed an arteriovenous malformation (AVM) in the left frontal lobe without evidence of bleeding and venous thrombosis. Subsequent Digital Subtraction Angiography (DSA) showed a small AVM with a compact high-flow nidus in the left frontal lobe fed by multiple branches from the left anterior cerebral artery (ACA) and middle cerebral artery (MCA). The AVM drained through four dilated and tortuous cortical veins into superior sagittal sinus as well as into the straight sinus (Grade 3 Spetzler–Martin). A diagnostic lumbar puncture revealed an opening pressure of 38 cm H₂O. The patient had no predisposing factors for intracranial hypertension. Based on these findings, the embolization of the AVM was considered treatment option. Complete occlusion of the nidus using Onyx glue was achieved in one session. One-week post intervention, the patient reported significant improvement of headache and blurred vision and intracranial pressure was 28 cm H₂O with lumbar puncture assessment. At the 1-month follow-up, bilateral pupil edema disappeared and intracranial pressure was 21 cm H₂O.

Case 2

A 15-year-old female patient was referred to our center with a history of headache, bilateral orbital pain, intermittent blurred vision, and right hand tingling. A brain MRI revealed multiple superficial flow voids in the left parietal lobe just posterior to the hand-area on the motor cortex. A DSA showed a large high-flow nidus AVM involving two compartments that were fed by the left MCA and ACA. It also contained two large intranidal aneurysms and had multiple draining veins to the superior sagittal sinus (SSS) and the left transverse-sigmoid sinus junction (Grade 3 Spetzler–Martin). Due to the bilateral papilledema and visual disturbance on ophthalmic exam, a lumbar puncture was performed and showed a pressure of 33 cm H₂O. Three days after admission, complete endovascular embolization of the AVM could be achieved at one session. The patient’s symptoms improved and intracranial pressure decreased to 27 cm H₂O after 1 week. At the 1-month follow-up examination, the bilateral papilledema was resolved and the intracranial pressure was 19 cm H₂O.

Case 3

A 39-year-old male patient presented with history of headache, intermittently blurred vision, and progressive visual acuity decrease in the right eye (best corrected visual acuity: 20/40). An ophthalmic examination showed right optic nerve atrophy and a normal left eye. A brain MRI revealed flow voids in the right posterior frontal lobe in close proximity to the leg motor cortex. A DSA showed an AVM nidus at the medial posterior of superior frontal gyrus, fed by multiple branches derived from the right ACA as well as right external carotid artery via the right middle meningeal artery. The AVM drained via cortical veins into the SSS (Grade 3 Spetzler–Martin). A lumbar puncture revealed an opening pressure of 31 cm H₂O. Because of the proximity of the AVM nidus to the motor cortex and en-passage feeder to the motor cortex, a partial AVM embolization with Onyx was performed and observation was considered. Lumbar CSF pressure decreased to 29 cm H₂O after 1 week and azetazolamide 250 mg was prescribed to treat the headaches and elevated ICP. After 1 month, the lumbar puncture showed that pressure decrease to 27 cm H₂O. Two months later, the lumbar puncture rose to 30 cm H₂O and the patient complained about headaches and azetazolamide intolerance. Another stage of embolization was considered for this patient. At second stage, near complete occlusion of the AVM nidus with preservation of en-passage artery could be achieved. The patient experienced no new neurological deficit and the headaches resolved. A subsequent lumbar puncture showed that the pressure normalized to 24 cm H₂O without medication. For complete occlusion, additional radiotherapy was performed. At the 6-month follow-up, bilateral papilledema disappeared and intracranial pressure was decreased.

Case 4

A 38-year-old female presented with history of chronic headaches and intermittent blurred vision that recently worsened with progressive visual disturbance and a right side visual field defect (right nasal quadrianopia). The fundoscopic examination showed bilateral optic disc edema. A brain MRI revealed flow voids in the right occipito-parietal region suspicious of an AVM nidus. The patient refused lumbar puncture for pressure measurement. A DSA showed a large high-flow AVM nidus fed by right MCA and posterior communicating artery (PCA) branches. The AVM had multiple draining veins into SSS and transverse-sigmoid junction (Grade 3 Spetzler–Martin). A near complete Onyx occlusion could be achieved in one session. The headache and visual disturbance improved and bilateral papilledema had resolved at the 1-month follow-up examination.

Discussion

In rare cases, unruptured AVMs can present with visual symptoms that are clinically and radiologically compatible with intracranial hypertension.^1–3 Although the definition of benign intracranial hypertension may not be correct in the presence of cerebrovascular lesions, a coexistence of these two processes is possible.^1,2 Abnormal drainage of cortical veins due to arterialization may be the underlying mechanism. A subsequent high pulse pressure in the subarachnoid space leads to increased cerebral pressure without affecting CSF resorption or cerebral blood volume.^2,3,5 The prompt treatment response in our patient population supports this hypothesis.

Literature review and treatment strategies

A review of the literature yielded a total of 26 similar cases (Table 1). All described treatment strategies can be divided into two principal categories: ICP lowering treatment and AVM treatment. Symptomatic medical treatment for benign intracranial hypertension alone consists of acetazolamide, diuretics, or corticosteroids. Surgical treatments include ventriculoperitoneal shunt, lumbo-peritoneal shunt, or optic nerve sheath fenestration. They were generally used if medical treatment failed.^{2,8,11,12,15,19–21} In some cases, however, despite treatment with ICP lowering drugs and even surgical CSF diversion without AVM treatment, symptoms did not improve (2, 10, and 17). In other reports, patients were initially treated successfully with medications, but later required surgical, neurointerventional, surgical, or radio-surgical treatment.^2,12 The cases initially treated with surgical ICP management appeared to yield better outcome than those with medical therapy only.^8,19

Table 1.

Summary of recent studies concerning intracranial hypertension and papilledema secondary to cerebral AVM in the worldwide.

Study	Symptom duration	Age (y)	Gender	Site of lesion	Feeder	Drainage	Treatment	One year outcome	LP pressure
Kosary 6	6 months	25	Male	Rt parietal	ACA	SSS	Surgical resection	Improved	N/A
Ito 7	1 month	12	Male	Rt frontal lobe	ACA and MCA	Cortical (SSS)	Surgical resection	N/A	N/A
Weisbay 8	4 years	40	Male	Rt parieto-occipital	ACA and PCA	N/A	LP shunt	N/A	N/A
Vassilouths 9	3 months	11	Male	Rt frontal	ACA	ISS and SSS	Surgical resection	Improvement	N/A
Vanderberg (Davf) 10	2 years	65	Male	Lt mastoid	Left external carotid artery and meningeal branch of vertebral artery	Strait sinus and vein of Galen	Corticosteroids and embolization	Improvement	N/A
Spallon 11	10 months	9	Male	Lt occipital	Occipital artery	Tentorial	Corticosteroid and diuretics	Improvement	19
Shiffer 3	2 months	31	Female	Rt frontal	MCA and ACA	SSS and internal cereberal	Surgical resection	Improvement	N/A
Barrow 12 (a)	3 months	21	Female	Rt frontal	ACA	SSS	Dexamethasone and azetazolamide, LP shunt, and surgical resection	Improvement after surgery	N/A
(b)	1 year	33	Female	Lt parietal	PCA, ACA, and MCA	SSS and Galen	Azetazolamide and furosemide	Not improved and LP serial After surgery hemiplegia and improvement	Initially = 50 After azetazolamide = 40
Chimowitz 2 (a)	5 years	19	Female	Rt parieto-occipital	ACA, PCA, and MCA	SSS	Embolization and surgical resection	Left hemianopia after surgery Improvement of pupil edema after 2 months	N/A
(b)	6 weeks	21	Female	Rt parietal	Rt MCA	SSS	Corticosteroid, diuretic, and surgical resection after 3 months	Optic atrophy	28
(c)	2 years	32	Female	Lt frontal	ACA and MCA	SSS	Azetazolamide, corticosterioid, furesmide for 2 years, and radiosurgery	No improvement	N/A
(d)	3 months	28	Male	Rt parietal	ACA and MCA	SSS	Embolization and surgery	Severe hemiparesia after surgery that improved after 4 months	N/A
(e)	Chronic headache	44	Female	Rt parieto-occipital	PCA and MCA	SSS	Corticosteroid, azetazolamide, and furosemide	Improvement	N/A
(f)	Acute (7 h)	24years	Male	Rt parieto-occipital	ACA, PCA, and MCA	SSS	Embolization and Surgery	Left hemianopia after surgery Improvement of pupil edema after surgery and permanent optic atrophy	N/A
Rosenfield 13	1 week	32	Male	Rt temporoparietal	MCA and anterior choroidal	Superficial (SSS)	Surgical resection	Hemineglect hemianopia	N/A
Cockerell (a)	2 months	35	Female	Left frontoparietal	ACA and MCA	SSS	Embolization	Improvement	28
(b) (Dural avf)	3 months	65	Male	Rt occipital	Rt occipital	Dural sinus	Embolization	Improvement	34
Kamite 14	N/A	14	Male	Lt temporal	Lt MCA and PCA	Transverse sinus	Surgical resection	Improvement	26
David 15	1 year	29	Male	Left temporoparietal	Lt MCA	Left transverse sinus cortical and deep	Optic nerve sheathe fenestration + medical therapy	Partial improvement	N/A
Verm 16	3 months	11	Female	Rt frontal	N/A	N/A	Partial embolization + oral prednisolone + VP shunt	Improvement	30
Vorstman 17	2 weeks	9yrsf	Female	AVM parietal	PCA	Superficial (SSS)	Endovascular, azetazolamide, and prednisolone	Improvement but mild optic atrophy after 3 months	40
Lai-wah 18 (a)	Acute	13	Male	Rt temporal	Rt MCA	Cortical deep	Azetazolamide radiosurgery	Cure of AVM after 2 years	36
(b)	Incidental finding	14	Male	Posterior fossa	Bilateral SCA	Strait sinus	Embolization	Symptoms improved	N/A
Baker 19	1 month	28	Male	N/A	N/A	N/A	VP shunt	N/A	“Elevated”
Kumar 20	3 months	23	Female	Rt parieto-occipital diffuse	Rt PCA Rt ACA MCA	Cortical (SSS) deep	Diuretics *	Improvement	N/A
Yuthagovit 1	1 week	16	Female	Rt temporal	Rt MCA Rt PCA	Transverse sinus and Rosenthal	Embolization	Improvement	N/A

Y: year; SSS: superior sagittal sinus; Rt: right; Lt: left; PCA: posterior communicating artery; MCA: middle cerebral artery; ACA: anterior cerebral artery; SRS: stereotactic radiosurgery; SCA: superior cerebellar artery; *proliferative angiopathy, refuse of surgical or endovascular treatment; #history of symptomatic AVM 1 year ago.

Overall, three case reports described good response to medical treatment while six cases required additional surgical intervention including CSF diversion, optic nerve sheath fenestration, or surgical resection of the AVM.^2,12,15,21 The outcome after CSF diversion was superior to medical treatment, but one patient required surgical resection of the AVM despite good functional CSF diversion. However, despite well controlled ICP, severe optic atrophy was associated with poor visual outcomes. ¹²

Surgical resection of the lesion

The majority of reported surgical treatments in patients with intracranial hypertension and an unruptured AVM were reported before the advent of curative endovascular AVM treatment.^{3,6,7,9,13,14}

Endovascular treatment

Due to recent technologic advances, endovascular therapy may be used as the first line treatment in certain cases. The important point for this method is the selection of partial or complete vascular lesion treatment. Although partial embolization sufficiently treats intracranial hypertension in some cases, supplementary treatments, surgical resection, or radiosurgery are required in other cases Optionally, initial endovascular treatment can be used for pre-operative embolization. ²

Based on these findings, we chose to recommend endovascular embolization as the option if feasible. Response to the endovascular treatment was fast and effective in our case series. Clinical improvement could be observed as early as the first postoperative day. After 1 week, the opening pressure on lumbar puncture was significantly reduced, indicating a decreased ICP.

In cases with complete AVM embolization, the outcome was excellent and did not require the adjustment of long-term medical treatment. Partial embolization was associated with partial resolution of symptomatology (Figures 1–4).

Figure 2.

{Case2}: A1 left ICA AP view pre-embolization, A2 left ICA lateral view pre-embolization, A3 left ICA AP view post-embolization, A4 left ICA Lateral view post-embolization, B1 right eye papilledema pre-embolization, B2 left eye papilledema pre-embolization, C1 right eye OCT resolved papilledema 1-month post-embolization, and C2 left eye OCT resolved papilledema 1-month post-embolization.

Figure 3.

{Case 3}: A1 right ECA lateral view pre-embolization, A2 right ECA lateral view post-embolization, A3 right ICA lateral view pre-embolization, A4 right ICA lateral view post-embolization, A5 right ICA AP view pre-embolization, A6 right ICA AP view post-embolization, B1 right eye optic atrophy pre-embolization, B2 left eye normal pre-embolization, C1 right eye OCT 1-month partial optic atrophy post-embolization, and C2 left eye OCT 1-month normal papilla post-embolization.

Figure 1.

{Case1}: A1 left ICA lateral view pre-embolization, A2 left ICA AP view pre-embolization, A3 left ICA Lateral view post-embolization, A4 left ICA AP view post-embolization, B1 right eye papilledema pre-embolization, B2 left eye papilledema pre-embolization, B3 right eye resolved papilledema 1-month post-embolization, B4 left eye resolved papilledema 1 month post-embolization, C1 right eye OCT 1-month post-embolization, and C2 left eye OCT 1-month post-embolization.

Figure 4.

{Case 4}: A1 right VA lateral view pre-embolization, A2 right VA AP view pre-embolization, A3 right ICA lateral view pre-embolization, A4 right ICA AP view pre-embolization, A5 right VA lateral view post-embolization, A6 right VA AP view post-embolization, A7 right ICA lateral view post-embolization, and A8 right ICA AP view post-embolization.

Conclusion

Our case series as well as a review of the literature indicated that intracranial hypertension might occur as a sequel of an unruptured supratentorial AVM. Increased ICP and papilledema without hydrocephalus may therefore be an indication for AVM treatment. Any delay in the treatment of such lesions may result in irreversible damages to the optic nerve. In these patients, endovascular treatment can be used safely as primary treatment if complete or near complete AVM occlusion can be achieved. However, if complete endovascular occlusion is not possible, complementary radiosurgery or primary surgical resection might be required.

ORCID iDs

Christoph J Griessenauer https://orcid.org/0000-0002-2952-3812

Abolghasem Mortazavi https://orcid.org/0000-0003-3279-6456