Intraorbital arteriovenous malformation: Case report

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Intraorbital Arteriovenous Malformation: Case Report Shushovan Chakrabortty, M .B .B .S., Tatsuya Nagashima, M .D., Ichiro Izawa, M.D., Yoshibumi Sekiya, M .D., Torao Sugiura, M .D., Masanori Inoue, M .D., Yukihiro Imai, M.D., Kazumasa Ehara, M.D., and Norihiko Tamaki, M .D. Departments of Neurosurgery (S .C ., T.N ., I .I., K.E., N.T .), Kobe University School of Medicine, Kobe, Japan

Chakrabortry S, Nagashima T, Izawa I, Sekiya Y, Sugiura T, Inoue M, Imai Y, Ehara K, Tamaki N . Intraorbital arteriovenous malformation : Case report . Surg Neurol 1993 ;40:320-5 . A case of intraorbital arteriovenous malformation presenting with visual loss, exophthalmos, and chemosis of the right eye is reported . Enhanced computer tomography and magnetic resonance imaging showed extraocular muscle enlargement and vascular abnormality in the right retrobulbar space . Angiography revealed an abnormal intraorbital vascular stain with an extremely dilated right ophthalmic artery . Total removal of the intraorbital contents was performed after unsuccessful endovascular and surgical treatment of arteriovenous malformation (AVM) . Histopathological examination disclosed an AVM in the retrobulbar fatty tissue with extension into the extraocular muscles and optic nerve .

Ophthalmology (Y .S ., T .S., M .I .),

and Pathology (Y .L),

patient was born in 1963, after a full-term, uncomplicated pregnancy. There was no history of orbital trauma and no family history of vascular disorders . At the age of 4, slight proptosis and conjunctival redness of the right eye were noticed, but there was no visual disturbance . When he was 26 years old, right-sided exophthalmos and conjunctival chemosis became progressive with rapid deterioration of vision, and the patient was admitted to the ophthalmology department of this hospital . Histopathological examination of a biopsy specimen of the lateral rectus muscle and retrobulbar fat revealed an AVM . By this time, despite conservative treatment with steroids, he developed complete loss of vision in the right eye, and was referred to our department. Examinations

wolos : Arteriovenous Malformation ; Optic nerve ; Orbital cavity ; Primitive ophthalmic artery KEY

Although intraorbital vascular malformations are a common cause of unilateral exophthalmos, true intraorbital arteriovenous malformations (AVM) are rare . A case of arteriovenous malformation in the right retrobulbar intraconal space with extension into the extraocular muscles and optic nerve is reported . With the experience of the present case and by an analysis of some previously reported cases, management strategy is also discussed .

Case Report A 27-year-old right-handed male was admitted to our department on September 4, 1990, because of visual loss, exophthalmos, and chemosis of the right eye . The

Address reprint requests to : Tatsuya Nagashima, M .D., Department of Neurosurgery, Kobe University School of Medicine, 5-l, Kusunokicho, 7-chome, Chuo-ku, 650 Kobe, Japan. Received September 23, 1992 ; accepted January 19, 1993 . 0 1993

by Elsevier Science Publishing Co ., Inc .

On admission, physical examination revealed marked exophthalmos, chemosis, a widened palpebral fissure, restricted extraocular movements in all directions, and complete loss of vision in the right eye . Eye positions were neutral, and pupils were isocoric and round . No bruits were audible over the right orbit . Neurological examination showed no other deficits except for those in the right eye . A computed tomographic (CT) scan revealed enlargement of the right extraocular muscles, and abnormally enhanced areas in the retrobulbar fat (Figure 1) . The T I -weighted magnetic resonance (MR) images showed right exophthalmos, extraocular muscle enlargement, and abnormal flow voids in the right retro-bulbar space representing abnormal vasculature (Figure 2 A and B) . A cerebral angiogram revealed an abnormal vascular stain in the right orbit fed by the right ophthalmic artery (Figure 3) . Clinical Course Clipping of the right ophthalmic artery was planned instead of embolization to avoid the risk of distant intra0090-3019/93/$6 .00



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ore 5) . On December 6, 1990, the patient underwent surgery through a transcranial extradural approach . Opening the roof of the orbit and laterally retracting the superior rectus muscle revealed many dilated and tortuous vessels . The primitive ophthalmic artery and most of the vascular mass embedded in the retro-bulbar fat were removed prior to orbital reconstruction . However, the cosmetic result was not satisfactory . On January 17, 1991, exenteration of the right intraorbital contents was performed at the ophthalmology department for cosmetic purposes .

Pathology

Figure

1 . Contrast-enhanced axial CT scan showing right-sided exophtbalmos, enlarged but nonenhanced right extraocular muscles, and abnormally enhanced areas (arrows) in the right retrobulbar intraconal fat .

cranial embolism . Accordingly, on September 17, 1990, clipping was performed through a right pterional approach . Postoperative angiograms revealed that new collateral feeders had developed from a persistent primitive ophthalmic artery (Figure 4 A), maxillary artery, and superficial temporal artery of the right side (Figure 4 B). On October 5, 1990, embolization of the feeders from the right external carotid artery was performed with polyvinyl alcohol particles . The postembolization angiogram revealed almost complete embolization (Fig-

Figure

2. (A) T,-weighted axial MR image demonstrating right exophthalmos, extraocular muscle enlargement, and serpiginous flow voids (arrows) in the right retrobulbar space, (B) T 5 -weighted coronal MR image s > g enlargement of the right extraocular muscles and an abnormal flow void (arrow) .

Preembolization histopathological findings were suggestive of AVM (Figure 6 A) . After embolization, the retrobulbar vascular lesion was composed of thickwalled vessels with collapsed and obliterated lumens (Figure 6 B). Embolization material was also seen in some blood vessels (Figure 6 C) . After the exenteration of the right globe, pathological examination demonstrated that the vascular lesion also extended into the right optic nerve (Figure 6 D) . Before any therapeutic procedures, histopathological findings were very typical for AVM, but after clipping the right ophthalmic artery and embolization of the feeders from the external carotid artery, most of the blood vessels of the lesion became thickened, collapsed, and sclerosed, making the distinction between an artery and a vein very difficult . These changes might have been due to the reduction in blood flow to the AVM and also due to the reactive effect of embolization . Intraorbital AVM located mainly into the retrobulbar intraconal fat extending into the optic nerve and extraocular muscles was the final diagnosis .



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Chakrabortty er al

malformations [9,20] . Pathological examination of AVMs reveals masses of arteries, "arteriolized veins," and veins . The component vessels vary greatly in size, but the larger vessels are always venous . There is no recognizable normal capillary bed in AVMs [12] .

Figure 3 . Lateral view of the right internal carotid angiogram showing an abnormal intraorbital vascular staining (arrowheads) and an extremely dilated right ophthalmic artery (arrow) .

Discussion Incidence and Pathological Classification There have been 20 previously reported cases of intraorbital AVM (Table 1) . Of these, three cases were diagnosed by both histopathology and angiography [4,19], seven cases by angiography alone [5,6,8,10,19], seven cases by pathology [13,19], and three cases by clinical suspicion alone [17,191 . On a pathological basis, vascular malformations can be classified into four groups : (1) AVMs; (2) venous angioma ; (3) cavernous angioma; and (4) capillary angioma [11,12) . In addition to these four groups, transitional forms also exist . Intraorbital capillary and cavernous angiomas are considered common [11 . Some authors consider congenital venous malformations to be the most frequent of intraorbital vascular

Clinical Features of Intraorbital AVM AVMs are congenital lesions that develop during the late somite stage in the fourth week of embryonic life [1-3] . They are clinically symptomatic and usually less progressive . The common symptoms and signs are conjunctival chemosis, proptosis, restricted extraocular movements, headache, secondary glaucoma, and dilatation of the veins of retina, conjunctiva, and eye lids . Visual disturbances may also occur, and they have some similarity to carotid cavernous fistula . Pulsating exophthalmos and bruits present only occasionally in intraorbital AVM as opposed to carotid cavernous fistula .

Diagnosis Although the differential diagnosis for unilateral exophthalmos is large, careful clinical examination, enhanced CT, MR imaging, orbital angiography, and ultrasonography have definite roles in the correct diagnosis of intraorbital AVM [6,9,10,13-16] . CT and MR imaging can

Figure 4 . (A) After clipping the right ophthalmic artery, right internal carotid angiogram showing collateral feeders (arrowheads) from a persistent primitive ophthalmic artery (arrow) . (B) Selective right external carotid angiogram showing collateralfe from the maxillary artery (arrowheads) and a dilated superficial temporal artery (arrows).



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technique . In cases

of

323

venous, capillary, and cavernous

angiomas, however, it reveals a vascular mass lesion . In the present case, the initial right internal carotid artery angiogram revealed a dilated ophthalmic artery . Immediately after clipping, new feeders developed from the right primitive ophthalmic artery, superficial temporal artery, and internal maxillary artery . These feeders were, therefore, functionally inactive before the clipping

of the

right ophthalmic artery, which was the dominant

feeder . The angiogram could not demonstrate any spe-

cific

drainage but many dilated veins were visualized

of the vascular lesion . They may have been occluded by either spontaneous thrombosis

during surgical removal

or after slight hemorrhage . The presence of an AVM in the orbit can be often part of more extensive vascular anomalies [18] . Of the 20 reported cases, four cases had other intracranial or extracranial vascular angiomas [6,19] . Extensive studies Figure 5 . Right common carotid digital subtraction angiogram showing almost complete embolization of the feeders from the superficial temporal artery (arrows) and maxillary artery (arrowheads) .

readily detect an intraorbital lesion, delineate the extent, and may characterize the type

CT

of

lesion. In most cases,

are, therefore, indicated to rule out other intracranial or extracranial vascular lesions when intraorbital vascular malformations are present .

Management of Intraorbital AVM The slow rate

of

progression and chance

of

spontane-

reveals exophthalmos, extraocular muscle enlarge-

ous thrombosis with a clinical cure sometimes favors

ment with variable enhancement [15], and vascular abnormalities such as a dilated superior ophthalmic vein .

a conservative approach [12,13] . Recent development of neuroradiological techniques for the exact localiza-

Orbital angiography demonstrates the feeders, drainers,

tion

and nidus

of the

AVM, particularly with the subtraction

of

vascular lesions and endovascular surgery have

improved the management strategy . Initial surgical

Table 1 . Previously Reported Cases of Intraorbital Arteriovenous Malformations case No. I 2 3 4 5 6

Authors) and Year Terry and Fred, 1938 Jacas et al, 1959 Krayenbuhl H, 1962 Levy and Zemek, 1966 Wolter JR, 1975

7

8 9 10 11 12 13 14 15 16 17 18 19 20

Murali et al, 1981 Howard et al, 1983 Muster and Kennerdell, 1983 Abbreviations. M, RE, right.

Lt, left ;

male ;

F,

Sex and Age (Years)

Onset (Years)

F, 23 F, 31 F, 42 M, 16 M, 52 M, 8 M, 36 F, 47 M, 38 M, 50 M,21 M, 74 M, 1 .7 M, 63 F, 26 F, 44 M, 40 M, 53 M, 19 M, 49

23 29 42 10 52 8 31 45 37 50 21 73 1 .6 53 26 44 40 51 17 49

Side Lt Lt Lt Lt Rt Lt Rt Lt Rt Lt RE

Rr Lt Rt Lt Both RE

Rt Rt Lt

Diagnosis

Treatment

Clinical Angio. Angio . Angio. Angio. Angio and Path Angio and Path Angio and clinical Path Path Clinical Path Clinical Path Path Path Angio Path Angio and Path Angio

Surgical removal Patient refused operation Ligation of Lt ECA, IMA Ligation of Lt ECA, ICA Patient refused operation Surgical removal Surgical removal Observation Partial removal Extensive biopsy Observation Enucleation Observation Surgical removal Surgical removal Surgical removal Observation Spontaneous thrombosis Embolization Embolization

female ; Angio, angiogram; Path, pathology ; ECA, external carotid artery ; IMA, internal maxillary artery ;

Result

ICA,

Improved Improved Not mentioned Improved Cured No change Not mentioned Not mentioned Improved Not mentioned Improved Improved Unchanged Improved Nor mentioned Improved Improved Nor mentioned internal carotid artery ;



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removal may be hazardous due to excessive bleeding from the lesion . Embolization reduces both the size and vascularity of the nidus, hence rendering surgical management more feasible [4] . For therapeutic purposes, AVM can be divided into two groups : malformations vascularized from the internal carotid artery and those vascularized from the external carotid artery [14] . Arterial embolization is possible only in malformations vascularized by branches of the external carotid artery . Purely intraorbital AVMs are mainly vascularized by the ophthalmic artery and cannot be subjected to arterial embolization . The feasibility of surgical removal

Chakrabortty et al

Figure 6. (A) Photomicrograph of the retrobulbar fat, taken from the biopsy material before embolization, showing artery (arrow), vein (arrowhead), thick-walled "arteriolized vein" (open arrow) and hemorrhage asteris , H & E, x 50 . (B) The rejected retrobulbar vascular lesion demonstraring many thick-walled vessels (arrows) with collapsed and obliterated lumens after staining with Elastica van Gieson (E .V .G .), x 88. (C) Histopathologicappearance of the extraocular muscles showing embolic materials (large arrows) inside an artery . Many thick-walled vascular structures were also seen (small arrows), E .V .G . . x 35 . (D) Photomicrograph of the right optic nerve showing numerous, densely arranged blood vessels occupying a considerable area of the optic nerve tissue . The walls of the vessels were thickened (arrowheads), and the lumens were collapsed (arrows) and almost obliterated in many places, E.V.G ., x 88 .



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and postoperative outcome depends mainly on location and extent . The previously

reported cases showed

some clinical improvement after surgical removal in a few cases, but the extent

of removal was not clearly

detailed . In the present case, there were errors in the embryologic development

of the ophthalmic artery, and as a

result, the right orbit was supplied by two arteries arising from the internal carotid siphon . At the stage

4- to 8-mm

of embryo, two primitive ophthalmic arteries-the

ventral and dorsal ophthalmic arteries-supply the orbital region [7] . At a later stage, the dorsal ophthalmic artery disappears at the level of the superior orbital fissure [7] . In our case, the persistent primitive opthalmic artery was the dorsal ophthalmic artery, which had not disappeared . The presence

of this primitive ophthal-

mic artery made the patient's condition more complicated, because clipping it was difficult and embolization

of the risk of distant intracranial of the rapid visual deterioration

was not justified because embolism . The causes

and subsequent right-sided blindness were compression

of the optic nerve by intraorbital venous congestion and massive AVM invasion of the optic nerve.

Conclusions The causes

of unilateral exophthalmos are many but

some are due to intraorbital vascular anomalies . Among these, intraorbital AVMs are rare . Radical extirpation of these malformations while preserving vision is obviously impossible when they extend into the optic nerve or retina . However, early and exact diagnosis and a multidisciplinary staged approach may make their removal safer and also reduce the threat to the patient's vision .

References 1 . Flanagan JC . Vascular problems of the orbit . Ophthalmology 1979 ;86:896-913 . 2 . GarretsonHO .Intracranialarteriovenousmalformations .In :Wilkins RE, Rengachary 55, eds . Neurosurgery . New York: McGraw-Hill, 1985 :1448-58.

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3 . Henderson JW . Vascular malformations . In : Henderson JW, ed . Orbital rumors, 2d ed . New York : Thieme-Stratton Inc ., 1980 :154-76 . 4 . Howard GM, Jakobiec FA, Michelsen WJ . Orbital arteriovenous malformation with secondary capillary angiomatosis treated by embolization with silastic liquid . Ophthalmology 1983 ; 90 :1136-9 . 5 . Jacas R, Ley A, Campillo D. Congenital intraorbital arteriovenous aneurysm. J Neurol Neurosurg Psychiatry 1959 ;22 :330-2 . 6 . Krayenbuhl H . The value of orbital angiography for diagnosis of unilateral exophthalmos. J . Neurosurg 1962 ;19 :289-301 . 7 . Lasjaunias P, Berenstein A . The internal maxillary system . In : Lasjaunias P, Berenstein A, eds . Surgical neuro-angiography, Vol . 1 . Functional anatomy of craniofacial arteries . Berlin, Heidelberg : Springer-Verlag, 1987 :33-122 . 8 . Levy JV, Zemek L . Ophthalmic Arteriovenous Malformation . Am J Ophthalmol 1966;62 :971-4 . 9 . Lloyd GAS . Vascular abnormalities in the orbit : CT and angiographic diagnosis . Orbit 1982 ;L45-54 . 10 . Moster MR, Kennerdell JS . B-Scan ultrasonic evaluation of a dilated superior ophthalmic vein in orbital and retro-orbital arteriovenous anomalies . J Clin Neuro Ophthalmol 19833 : 105-8 . 11 . McCormick WE The pathology of vascular ("Arreriovenous") malformations. J Neurosurg 1966 ;24 :807-16 . 12 . McCormick WF . The pathology of Angiomas . In: Fein JM, Flamm ES, eds . Cerebrovascular surgery . New York : Springer-Verlag, 19851073-95 . 13 . Murali R, Berenstein A, Hirschfeld A . Intraorbital arteriovenous malformation with spontaneous thrombosis . Ann Ophthalmol 1981 ;13 :457-9 . 14 . Peeters H.M . Vascular malformations as the cause of unilateral exophthalmus . Diagnostic and therapeutic considerations . Diagnostic Imaging 1982 ;51 :1-7 . 15 . Rothfus WE, Curtin HD. Extraocular muscle enlargement: A CT review . Radiology 1984 ;l51 :677-81 . 16 . Tan WS, Wilbur AC, Mafee MF . The role of the neuroradiologist in vascular disorders involving the orbit. Radiol Clin North Am 1987 ;25 :849-61 . 17 . Terry TL, Fred GB . Abnormal arteriovenous communication in the orbit involving the angular vein . Report of a case . Arch Ophthalmol 1938 ;19:90-4. 18 . Walsh FB, Hoyt WE Tumors and hamartomas of blood vessels, In : Kist K, ed . Walsh and Hoyt's clinical neuro-ophthalmology, 4th. ed . Baltimore : Williams and Wilkins, 1988 :1485-542 . 19 . WolterjR . Arteriovenous fistulas involving the eye region . J Pediatr Ophthalmol 1975 ;12 :22-39 . 20 . Wright JE . Orbital vascular anomalies . Ophthalmol Otolaryngol 1974 ;78 :606-16 .