Endovascular treatment evolution for pure intraorbital arteriovenous fistula: Three case reports and literature review

Abstract

Background and importance

Intraorbital arteriovenous fistulas (IOAVFs) are rare and cause eye redness, exophthalmos, blurry vision and bruit. Whereas in the past they were treated conservatively, surgically or transarterially, recent developments in transvenous embolization have improved their treatment. In this paper the authors report three cases of IOAVFs treated endovascularly and review the evolution of treatment options.

Methods

Three cases of purely IOAVF enrolled in our center were reported and a PubMed literature search was performed using “pure intraorbital arteriovenous fistula” and “arteriovenous fistula of the optic nerve sheath.” A total of 21 papers were reviewed in full, focusing primarily on the treatment and outcomes.

Results

A total of 26 patients were obtained, including our three patients and 23 patients reported in the literature. In nine patients treated conservatively, four spontaneous occlusions, one visual deterioration and four cases with unknown outcome were reported. In another 18 patients, 29 therapies (including five surgical treatment, 11 transarterial embolizations and 13 transvenous embolizations) were attempted and resulted in 12 cures, five visual deteriorations and one without reported outcome. More recently, transvenous embolization has become the mainstay of IOAVF treatment. Of the 21 patients assessed between 2000 and 2013, a transvenous approach was attempted in 13 patients; nine patients were cured without any adverse events.

Conclusion

Development and improvement of transvenous techniques are found to be safe and effective for patients with IOAVF.

Introduction

Intraorbital arteriovenous fistulas (IOAVFs) are very rare arteriovenous shunts purely within the orbit that do not connect to the cavernous sinus and are usually supplied by branches of the ophthalmic artery (OA), distal internal maxillary artery (IMA) or middle meningeal artery (MMA) and drain into the dilated superior ophthalmic vein (SOV) or inferior ophthalmic vein (IOV) or their distributions.¹ The etiological basis of IOAVF could be traumatic injury; however, most of them are spontaneous.² IOAVFs increase intraorbital vein pressure and varix formation and cause eye redness, exophthalmos, loss of visual acuity and bruit.³ In the past, they were treated conservatively, surgically or transarterially, and usually resulted in failure and loss of visual acuity; recent developments in transvenous embolization have improved their treatment.^2–7 In this paper, we describe three cases of IOAVF treated endovascularly and review their clinical presentation, history of treatment options, and recent advances in endovascular management.

Methods

Three cases of pure IOAVF enrolled in our center were reported and a PubMed literature search was performed using “pure intraorbital arteriovenous fistula” and “arteriovenous fistula of the optic nerve sheath” up to October 2014 (Table 1). A total of 21 papers were reviewed in full, focusing primarily on the treatment and outcomes. The goal of the search was to assess the evolution of treatment options for IOAVFs over time. Given the rarity of IOAVFs, this paper provides valuable information regarding the natural history, treatment, and outcomes of this condition.

Table 1.

Case reports of purely intraorbital arteriovenous fistula from the literature.

Case reports	Year	Sex	Age	Presentation	Pathogenesis	Feeding artery	Draining vein	Initial diagnosis	Treatment	Results	Complications	Outcome
Rengachary and Kishore8	1978	M	63	NA	Spontaneous	OA, aneurysm rupture	SOV	NA	Conservative	NA	No	NA
Freitas et al.9	1983	M	39	Exophthalmos and bruit	Penetrating injury	OA, false aneurysm	SOV	Angiography	Spontaneous closure after angiography	Complete	No	Complete occlusion
Rootman et al.10	1992	M	31	NA	Blunt trauma	OA, STA	FV	NA	Surgical resection after arterial embolization	NA	NA	NA
Chakrabortty et al.11	1993	NA	NA	Visual loss, exophthalmos	Spontaneous	OA	NA	CTA, MRI, DSA	Unsuccessful arterial embolization and surgical treatment	Complete	Total removal of the intraorbital contents	NA
Ohtsuka and Hashimoto12	1999	F	73	Exophthalmos	Spontaneous	Branches of OA and FA	SOV	CTA	Conservative	NA	NA	NA
To and Chan13	2000	M	75	NA	Penetrating injury	NA	NA	NA	Conservative	NA	NA	NA
Kim and Kosmorsky1	2000	M	65	Redness, diplopia	Spontaneous	Ethmoidal branches of OA and deep temporal artery from IMA	SOV	MRI, DSA	PVA embolization via IMA and OA	Occlusion of superotemporal branch of retinal artery	Partial	Visual deficit
Huna-Baron et al.14	2000	M	66	Pain, redness, exophthalmos	Spontaneous	OA and IMA supplier via OA	Drained to CS post eriorly	MRI, DSA	PVA embolization via IMA and failure of transvenous and orbitotomy	partial	No	After two years, visual acuity in left eye was hand movements
		M	71	Exophthalmos	Spontaneous	OA and ECA via collaterals to OA	NA	DSA	Compression of cervical carotid artery	No	No	After one year, vision deteriorated
Frankefort et al.15	2005	F	84	Redness, exophthalmos	Spontaneous	Meningeal branches of ICA	Orbital vein	NA	Conservative	NA	NA	NA
Subramanian et al.16	2005	M	33	Redness, pain, diplopia	Spontaneous	OA and IMA	IOV	MRI, DSA	After failure of IPS and FV, surgical exposure of SOV and embolization	Complete	No	Resolved completely. No residual fistula on three-month follow-up DSA
Hamada et al.4	2006	M	55	Upper lid swelling, redness, exophthalmos	Spontaneous	OA	SOV	DSA	Surgical exposure of SOV and embolization of SOV using oxidized cellulose (Surgicel)	Complete	No	After two months, all symptoms disappeared
Caragine et al.6	2006	F	51	Redness, exophthalmos	Spontaneous	OA and anterior branch of MMA	SOV	MRI, DSA	Partial embolization via MMA and coil embolization via FV	Complete	No	After one month, completely resolved
		F	63	Redness, exophthalmos, blurry vision, and bruit.	Spontaneous	Infraorbital artery of IMA	IOV	MRI, DSA	FV-angular vein -SOV-IOV and coil embolization	Complete	No	After three months, completely resolved
Yazici et al.17	2007	F	13	Exophthalmos	Penetrating Injury	OA	SOV	CTA, Doppler ultrason ography	Spontaneous occlusion after failure of femoral vein approach	Complete	No	After 23 months without recurrence
Cheng et al.18	2009	M	50	Blurred vision, exophthalmos	Spontaneous	OA	SOV and IOV	MRI	Conservative because of technical difficulty and high risk	Complete	No	After six months, vision and symptoms improved
Lin et al.5	2010	M	61	Redness, exophthalmos	Spontaneous	OA	A branch of SOV	Duplex orbital examinations	Onyx18 embolization via the FV	Complete	No	After six months, chemosis completely resolved and visual acuity improved
Sato et al.19	2011	M	53	Exophthalmos, pain	Spontaneous	OA	SOV	DSA	30% and 25% NBCA embolization via OA	Complete	No	After one year, complete disappearance of AVM
Kirsch and Henkes2	2011	NA	NA	Visual loss, intraorbital hematoma	Spontaneous	OA, aneurysm rupture	Cortical drain age	DSA	Coil occlusion of aneurysm and transvenous treatment of AVF	Complete	No	NA
Wigton et al.20	2012	M	61	Blurred vision, exophthalmos	Spontaneous	Superior OA	SOV	DSA	Lateral orbitotomy	Complete	No	After four months, vision improved
Williamson et al.3	2013	F	81	Blurry vision, diplopia	Spontaneous	OA	SOV	MRI, DSA	IPS-CS approach and coil embolization	Complete	No	After three weeks, blurry vision and ocular findings returned to normal
Naqvi et al.7	2013	M	72	Redness, exophthalmos	Spontaneous	Ethmoidal branches of OA	SOV	DSA	Surgical exposure of SOV coil embolization	Complete	No	After six months, visual acuity remained unchanged
Mishra et al.21	2013	F	50	Redness, exophthalmos, blurry vision, and pain	Spontaneous	ICA	SOV	CTA	Fronto-orbital craniotomy	Complete	No	After two months, all symptoms disappeared
Our three cases		F	52	Exophthalmos	Spontaneous	OA, ICA,MMA,IMA	SOV	DSA	Coil embolization of MMA after failure of FV	Partial	No	After 11 years, symptom disappeared
		M	52	Redness, exophthalmos	Spontaneous	OA	SOV	DSA	Onyx18 embolization via OA	Complete	Blindness	Blindness did not improve
		M	68	Visual loss, redness, exophthalmos	Spontaneous	OA	IOV	DSA	Onyx18 embolization by direct puncture of IOV	Complete	None	After five months, all symptoms disappeared

M: male; F: female; NA: not available; OA: ophthalmic artery; SOV: superior ophthalmic vein; STA: superficial temporal artery; FV: facial vein; CTA: computed tomography angiography; MRI: magnetic resonance image; DSA: digital subtracted angiography; FA: facial artery; IMA: internal maxillary artery; CS: cavernous sinus; PVA: polyvinyl alcohol; ECA: external carotid artery; IOV: inferior ophthalmic vein; IPS: inferior petrosal sinus; ICA: internal carotid artery; MMA: middle meningeal artery; NBCA: n-butyl cyanoacrylate.

Results

A total of 26 patients were obtained, including our three patients and 23 patients reported in the literature up to October 2014. In four (15.4%) patients, IOAVF was caused by orbit injury and was spontaneous in 22 (84.6%) patients, among whom two OA (9.0%) aneurysm ruptures were revealed. Patient ages ranged from 33 to 84 years (mean 61.2 years) for spontaneous patients and ranged from 13 to 75 years (mean 39.5 years) for traumatic patients (p = 0.014). We found a significant male predominance for IOAVF (male:female = 2:1). Loss of visual acuity was observed in 33.3% spontaneous IOAVF patients, exophthalmos in 79.0%, eye redness in 50.0%, diplopia in 12.4%, orbital pain in 12.4%, bruits in 8.3% and intraorbital hematoma in 4.1%.

Table 1 presents the data for various treatment options from 1978 to 2013. In this section, the treatment of 26 patients with IOAVFs was examined, and although several treatment options were presented, transvenous embolization was the most frequently chosen treatment. Early attempts at transarterial embolization and surgery of IOAVF were found to be considerably less successful, with very high risk (Table 2). Thirteen patients who underwent transvenous embolization between 2000 and 2013, including femoral vein approach, surgical access to SOV and direct puncture of SOV or IOV, were found to have a cure rate of 70%, without any adverse events. In contrast, in early conservative, surgical and transarterial groups, the cure rate was found to be 35% with a 30% visual deterioration rate. In univariate analysis, transvenous treatments were associated with a higher cure rate (p = 0.005, odds ratio (OR) 22.500, 95% confidence interval (CI) (2.105-240.483)) and good visual outcome (p = 0.029, OR 1.429, 95% CI (1.072-1.903)).

Table 2.

The relative effectiveness of various treatments for IOAVF.

Years	Treatments	No. of patients	Cure	Visual deterioration	Failure/Not reported
1978∼2009	Conservative	9	3	1	5
1992∼2013	Surgical	5	2	2	1
2000∼2011	Transarterial (PVA, Coil 1 or Onyx)	11	1	3	7
2000∼2012	Transvenous (surgical exposure, direct puncture, transfemoral vein)	13	9	0	4

IOAVF: intraorbital arteriovenous fistula; PVA: polyvinyl alcohol.

Case descriptions

Case 1

A 52-year-old woman, who presented with a four-month history of exophthalmos of the right eye, was admitted in 2003. There was no history of orbital trauma. Digital subtraction angiogram revealed intraorbital multiple arteriovenous shunts supplied by the right OA, meningohypophyseal trunk, MMA and IMA and draining into the SOV, which was grossly dilated and tortuous. The SOV drained anteriorly into the facial vein (FV). No nidus and no communication into the cavernous sinus were observed. Transvenous embolization via the femoral vein approach was attempted but failed and transarterial coil embolization was performed via the MMA, which resulted in partial embolization of the fistula. This patient was contacted by telephone in 2014 and her symptom had disappeared without any visual deficits.

Case 2

A 52-year-old man, who presented with a one-month history of proptosis and chemosis of the right eye, was admitted in 2009. There was no history of orbital trauma. Digital subtraction angiogram revealed intraorbital arteriovenous fistula supplied by the right OA and draining into the SOV (Figure 1(a)). The SOV drained anteriorly into several small tributaries with slow outflow (Figure 1(b)). Transarterial Onyx18 embolization was performed via the OA, which resulted in occlusion of the OA and the fistula (not shown). This patient suffered blindness of the right eye after procedure.

Figure 1.

A 52-year -old man presented with right eye redness and exophthalmos. (a) Right carotid artery angiogram, early arterial phase (lateral view). (b) Right carotid artery angiogram, late arterial phase (lateral view). The IOAVF was supplied by small branches of the OA and drained by the SOV slowly. This IOAVF was completely occluded by transarterial Onyx18 embolization via the OA but the retinal artery was also occluded, and he developed blindness of the right eye after the procedure. IOAVF: intraorbital arteriovenous fistula; OA: ophthalmic artery; SOV: superior ophthalmic vein.

Case 3

A 68-year-old man, who presented with a nine-month history of proptosis, chemosis and a five-month history of blindness of the left eye, was admitted in 2012. There was no history of orbital trauma. Digital subtraction angiogram revealed an intraorbital arteriovenous shunt between small branches of the left OA and the IOV, which refluxed into the SOV without communication with the cavernous sinus (Figure 2(a)). The IOV pouch was directly punctured and transvenous Onyx18 embolization of the IOV was performed, which resulted in complete occlusion of the fistula (Figure 2(b)). After five months, all his symptoms disappeared and no recurrence of the fistula was observed.

Figure 2.

A 68-year-old man presented with left visual loss, exophthalmos and eye redness. (a) Left carotid artery angiograms, early arterial phase (lateral view) and late arterial phase (lateral view). The IOAVF was supplied by small branches of the OA and drained by the IOV slowly to the SOV. (b) The IOV was directly punctured by a needle, a microcatheter was inserted through the needle and Onyx was injected. The left carotid artery angiogram, lateral view, showed complete occlusion of the IOAVF. Lateral view of unsubtracted angiogram showed the Onyx cast. After five months, all his symptoms disappeared and no recurrence of the fistula was observed. IOAVF: intraorbital arteriovenous fistula; IOV: inferior ophthalmic vein; OA: ophthalmic artery; SOV: superior ophthalmic vein.

Discussion

IOAVF may exacerbate intraorbital venous hypertension and increase the risk of visual deterioration. These patients manifest with symptoms related to ocular venous congestion, including eye redness, exophthalmos, and loss of visual acuity, diplopia, orbital pain, bruits and intraorbital hematoma. Although IOAVFs may present symptoms mimicking those of spontaneous carotid cavernous fistula,^22,23 IOAVFs lead to as high as 30% visual deterioration because they involve a direct connection from the ophthalmic artery to the ophthalmic vein.

The etiological basis of IOAVFs could be traumatic injury; however, most of them are spontaneous and OA aneurysm rupture may be found in these cases.² These lesions have been treated conservatively as well as by both open surgical and endovascular techniques. Advances in transvenous techniques have substantially improved outcomes. The first reported transvenous technique in IOAVF treatment was in 2000 by Huna-Baron et al.,¹⁴ but failed and their patient was treated by orbitotomy. In 2005, Subramanian et al.¹⁶ surgically exposed the SOV to embolize the IOAVF after failure of the femoral vein approach. As endovascular techniques continued to improve over the following years, successful cases were reported.^2–7 IOAVF did not communicate to cavernous sinus; in such circumstances, the IOAVF usually cannot be reached via the inferior petrosal sinus and FV and femoral vein approaches.¹⁴ Direct surgical exposure and cannulation of the SOV provides an alternative venous access if IOAVFs cannot be approached.^4,7,16,23 In some cases, such as our case 3, in which the IOV and SOV were both thrombosed and stenosed, surgical exposure of the superior ophthalmic vein will be very difficult. In such cases, we chose direct transorbit puncture of the IOV for Onyx embolization.²⁴

Despite advances in microsurgical techniques, surgical treatment of IOAVFs is indicated after failure of endovascular attempts and conservative treatment and is rarely indicated as the first option. Surgical approaches vary widely and each carries its own set of potential problems, such as lateral orbitotomy, fronto-orbital craniotomy and total removal of the intraorbital contents.^11,20,21 Today, surgical treatment is generally used only in cases of embolization and conservative treatment failure, or for the evacuation of giant thrombosed varix.²¹

Spontaneous thrombosis of lesions has also been known to occur,⁹ but does not constitute an effective therapeutic strategy, because it is quite rare and often results in visual deficits.¹⁴ In case reports, the outcome of four out of eight cases treated conservatively has not been reported.^8,13,15,17 Conservative treatment can be used in patients without significant loss of visual function and small IOAVFs, which were technically difficult and high risk.¹⁸

Because of the close proximity of the arterial feeder to the central retinal artery, and the tiny caliber of the draining branches of the superior ophthalmic vein, transarterial embolization may result in retinal artery occlusion.^1,5,7 In the case reports, six transarterial embolizations were attempted, resulting in three deteriorations of visual function, five partial occlusions and only one patient cure using diluted glue.¹⁹ Traditionally, n-butyl cyanoacrylate (NBCA) has been used as the embolic agent in the transarterial approach, but recently Onyx has gained popularity as well.²⁵ Embolization with NBCA can permanently occlude vessels, and can even potentially cure small fistulas, Onyx, however, predisposes to reflux proximally to the lesion and occlusion of the central retinal artery, which was demonstrated in our Case 2. Therefore, transarterial embolization should be avoided as far as possible in IOAVF treatment, and diluted NBCA is appropriate if it is attempted.

Currently, the optimal approach for treating IOAVFs is transvenous therapy. There are three main approaches to percutaneous intravenous embolization: femoral vein, surgical access to the SOV and direct puncture of the SOV or IOV. When the transvenous technique is used, occlusion of the IOAVF is obtained by packing the venous pouch with materials such as coils, oxidized cellulose (Surgicel) and Onyx.^3–6,26,27 Some authors treating IOAVFs use both transvenous and transarterial approaches, depending on the angioarchitecture of the lesion, such as OA aneurysm rupture.^2,9 However, many groups reserve the transvenous route for those cases in which transarterial embolization has failed or is unfeasible.^6,10 In this review, percutaneous transvenous embolization was used to treat 13 cases of IOAVFs, resulting in nine cases of complete improvement of visual function and no major complications.

Conclusion

Conservative treatment is recommended when clinical symptoms are mild. Cases of severe diplopia and visual deterioration should be treated. Development and improvement of transvenous techniques have been found to be safe and effective for patients with IOAVF.

Conflict of interest

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.