a microsurgical study of the anatomy and course of the ophthalmic

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142 J. Neurosurg. / Volume 106 / January, 2007 ITH recent endovascular technical advances, em- bolization of vascular and neoplastic lesions sup- plied by the OphA and its branches is common. Authors of numerous studies have detailed the angiograph- ic anatomy of the OphA and its branches. 13,31 However, the microsurgical anatomy of this important artery has not been investigated in detail. Furthermore, there are variable connections between OphA branches and branches of the MMA that clinically are critically important and explain the occasional occurrence of visual impairment and blind- ness following the embolization of lesions supplied by the MMA. 17 The frequency and pattern of these anastomotic channels have not been systematically examined. 16,18 The purpose of this study is to describe the microsurgical anato- my of the OphA and its branches, with particular attention to reciprocal connections with the MMA. Materials and Methods The course of the OphA and the MMA blood supply to the orbit were examined bilaterally in seven adult cadaveric heads (injected with colored fluid) using a surgical microscope (Wild M695, Leica Microsystems) at a magnification of 3 to 40. The anatomical dissec- tions were performed with microsurgical instruments and a high- speed drill when required. Digital photographs were taken at each step of the dissection. All measurements were performed with an electronic digimatic caliper ( 0.01 mm). Results Osseous Relationships The OphA, the recurrent meningeal artery, and the me- ningolacrimal artery (when present) enter the orbit through the optic canal, the SOF, and the meningolacrimal canal (when present), respectively (Fig. 1). The optic canal, which allows passage of the ON and the OphA, lies between the superior and inferior roots of the anterior clinoid process (Fig. 1A). The superior root forms the roof of the optic ca- nal and continues medially to form the planum sphenoidale (Fig. 1A). The inferior root (or optic strut) constitutes the in- ferolateral wall of the optic canal and separates the optic canal from the SOF (Fig. 1A). Both proximal (intracranial) and distal (intraorbital) openings of the optic canal are ellip- tical in shape. The length of the optic canal varies from 5 to 11 mm (mean 8 mm). The groove for the MMA starts at the foramen spinosum and then divides into posterior (parietal) and anterior (fron- tal) furrows 10 to 25 mm (mean 18 mm) anterolateral to the foramen spinosum (Fig. 1B). The frontal groove is larger, J Neurosurg 106:142–150, 2007 A microsurgical study of the anatomy and course of the ophthalmic artery and its possibly dangerous anastomoses P AOLO PERRINI, M.D., 1,3 ANDREA CARDIA, M.D., 1,4 KENNETH FRASER, M.D., 2 AND GIUSEPPE LANZINO, M.D. 1,2 1 Microneurosurgical Laboratory, Department of Neurosurgery, and 2 Department of Radiology, University of Illinois College of Medicine at Peoria, Illinois; 3 Neurosurgical Department, University of Florence; and 4 Neurosurgical Department, Galeazzi Hospital, Milan, Italy Object. The authors studied the microsurgical anatomy of the ophthalmic artery (OphA), paying particular attention to its possibly dangerous anastomoses with the middle meningeal artery (MMA). Methods. The microsurgical anatomy of the OphA and its anastomoses with the MMA were studied in 14 vessels from seven adult cadaveric heads. The origination order of the OphA branches varies in relation to whether the artery, along its intraorbital course, crosses above or below the optic nerve (ON). The central retinal artery is the first branch to course from the OphA when it crosses over the ON, and it is the second branch to course from the OphA when the artery crosses under the ON. Anastomoses between branches of the MMA and the OphA were present in the majority of the specimens examined. Conclusions. Detailed knowledge of the microanatomy of the OphA and recognition of anastomoses between the ex- ternal carotid artery and the OphA are critically important in avoiding disastrous complications during endovascular procedures. KEY WORDS middle meningeal artery ophthalmic artery orbit microsurgical anatomy embolization W Abbreviations used in this paper: CRA = central retinal artery; ECA = external carotid artery; ICA = internal CA; MMA = middle meningeal artery; ON = optic nerve; OphA = ophthalmic artery; SOF = superior orbital fissure.

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Page 1: A microsurgical study of the anatomy and course of the ophthalmic

142 J. Neurosurg. / Volume 106 / January, 2007

ITH recent endovascular technical advances, em-bolization of vascular and neoplastic lesions sup-plied by the OphA and its branches is common.

Authors of numerous studies have detailed the angiograph-ic anatomy of the OphA and its branches.13,31 However,the microsurgical anatomy of this important artery has notbeen investigated in detail. Furthermore, there are variableconnections between OphA branches and branches of theMMA that clinically are critically important and explain the occasional occurrence of visual impairment and blind-ness following the embolization of lesions supplied by theMMA.17 The frequency and pattern of these anastomoticchannels have not been systematically examined.16,18 Thepurpose of this study is to describe the microsurgical anato-my of the OphA and its branches, with particular attentionto reciprocal connections with the MMA.

Materials and MethodsThe course of the OphA and the MMA blood supply to the orbit

were examined bilaterally in seven adult cadaveric heads (injectedwith colored fluid) using a surgical microscope (Wild M695, Leica

Microsystems) at a magnification of 3 to 40. The anatomical dissec-tions were performed with microsurgical instruments and a high-speed drill when required. Digital photographs were taken at eachstep of the dissection. All measurements were performed with anelectronic digimatic caliper (6 0.01 mm).

Results

Osseous Relationships

The OphA, the recurrent meningeal artery, and the me-ningolacrimal artery (when present) enter the orbit throughthe optic canal, the SOF, and the meningolacrimal canal(when present), respectively (Fig. 1). The optic canal, whichallows passage of the ON and the OphA, lies between thesuperior and inferior roots of the anterior clinoid process(Fig. 1A). The superior root forms the roof of the optic ca-nal and continues medially to form the planum sphenoidale(Fig. 1A). The inferior root (or optic strut) constitutes the in-ferolateral wall of the optic canal and separates the opticcanal from the SOF (Fig. 1A). Both proximal (intracranial)and distal (intraorbital) openings of the optic canal are ellip-tical in shape. The length of the optic canal varies from 5 to11 mm (mean 8 mm).

The groove for the MMA starts at the foramen spinosumand then divides into posterior (parietal) and anterior (fron-tal) furrows 10 to 25 mm (mean 18 mm) anterolateral to theforamen spinosum (Fig. 1B). The frontal groove is larger,

J Neurosurg 106:142–150, 2007

A microsurgical study of the anatomy and course of theophthalmic artery and its possibly dangerous anastomoses

PAOLO PERRINI, M.D.,1,3 ANDREA CARDIA, M.D.,1,4 KENNETH FRASER, M.D.,2

AND GIUSEPPE LANZINO, M.D.1,2

1Microneurosurgical Laboratory, Department of Neurosurgery, and 2Department of Radiology,University of Illinois College of Medicine at Peoria, Illinois; 3Neurosurgical Department, University ofFlorence; and 4Neurosurgical Department, Galeazzi Hospital, Milan, Italy

Object. The authors studied the microsurgical anatomy of the ophthalmic artery (OphA), paying particular attentionto its possibly dangerous anastomoses with the middle meningeal artery (MMA).

Methods. The microsurgical anatomy of the OphA and its anastomoses with the MMA were studied in 14 vesselsfrom seven adult cadaveric heads. The origination order of the OphA branches varies in relation to whether the artery,along its intraorbital course, crosses above or below the optic nerve (ON). The central retinal artery is the first branchto course from the OphA when it crosses over the ON, and it is the second branch to course from the OphA when theartery crosses under the ON. Anastomoses between branches of the MMA and the OphA were present in the majorityof the specimens examined.

Conclusions. Detailed knowledge of the microanatomy of the OphA and recognition of anastomoses between the ex-ternal carotid artery and the OphA are critically important in avoiding disastrous complications during endovascularprocedures.

KEY WORDS • middle meningeal artery • ophthalmic artery • orbit •microsurgical anatomy • embolization

W

Abbreviations used in this paper: CRA = central retinal artery;ECA = external carotid artery; ICA = internal CA; MMA = middlemeningeal artery; ON = optic nerve; OphA = ophthalmic artery;SOF = superior orbital fissure.

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crosses the greater wing of the middle cranial fossa, andusually divides into the smaller medial and lateral grooves(Fig. 1B). The medial division of the frontal groove is usu-ally smaller, originates 5 to 15 mm (mean 8 mm) behindthe lesser wing and courses toward the lacrimal foramen(Fig. 1B) (also named the Hyrtl, meningolacrimal, cranio-orbital, meningoorbital, and stapedial–ophthalmo–lacrimalforamen), which accommodates the meningolacrimal ar-tery. In general, the existence of the lacrimal foramen is aninconsistent finding, occurring bilaterally in only two of thespecimens studied. When present, it is ovoidal and lies 5to 10 mm (mean 7 mm) laterally to the SOF and below thelesser wing (Fig. 1A). In the remaining specimens withouta true foramen, several small foramina were found in thesame general area, through which very small intraosseousbranches of the MMA enter the orbit.

From the area of the lacrimal foramina, a constant grooveruns medially to the narrow lateral apex of the SOF (Fig. 1Aand B). In this groove courses the recurrent meningeal ar-tery. Often the sharp lateral margin of the SOF presents a

notch for the recurrent meningeal artery, which supplies thedura mater of the SOF and the adjacent periorbita and thenanastomoses with the lacrimal artery (a branch of theOphA). In an anterior view of the orbit, the superior obitalfissure is posterior and medial to the lacrimal foramen,which when present is located along the superior edge of thelateral wall of the orbit (Fig. 1C). The anterior and posteri-or ethmoidal foramina pass through the frontoethmoidal su-ture at the junction of the roof and the medial wall of the or-bit (Fig. 1C).

Arterial Relationships

Origin and Courses of the OphA. On all cadaver sides butone, the OphA arose in the intradural space at an acute anglefrom the superomedial aspect of the anterior bend of theICA, just above the distal dural ring (Fig. 2). At its ori-gin, the OphA (mean outer diameter 1.6 mm, range 1.5–1.8mm) is located inferomedial to the ON, behind the op-tic canal. In only one specimen did the OphAs on both

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FIG. 1. Photographs showing the various osseous relation-ships in the study. A: Intracranial view of the right middlefossa, sphenoid ridge, and anterior clinoid process. Note thelocation of the optic canal and the lacrimal foramen. B: Su-peroposterior view of the right middle cranial fossa showingthe grooves of the MMA. The recurrent meningeal arterycourses into an osseous groove extending downward fromthe medial aspect of the lacrimal foramen to the lateral apexof the SOF. C: Anterior view of the right orbit. The opticcanal opens into the superomedial aspect of the orbital apex.Note the location of the SOF and the anterior and posteriorethmoidal foramina. A. = artery; Ant. = anterior; Clin. = cli-noid; Eth. = ethmoidal; Fiss. = fissure; For. = foramen; Inf. =inferior; Lac. = lacrimal; Men. = meningeal; Mid. = middle;Orb. = orbital; Post = posterior; Sup. = superior.

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sides give rise to intracranial perforating branches directedtoward the ventral aspect of the ON (Fig. 2C). Five mil-limeters (range 2.8–6.5 mm) from its origin, the OphApierces the dural sheath of the ON along its inferolateral as-pect and enters the optic canal (intracanalicular course). TheOphA in its intracanalicular course is embedded in the duralsheath of the ON, coursing along its inferolateral aspect.The OphA exits the optic canal inferolateral to the ON andemerges from the optic sheath. In one specimen, the OphAon one side arose from the clinoid segment of the ICA andentered the orbit through the medial aspect of the SOF.

Intraorbital Course. After passing through the optic fora-men and the anular tendon, the OphA continues its courseinferolaterally to the ON. According to previous descrip-tions, the intraorbital OphA can be divided into threesegments9 (Fig. 3A). The first segment runs along the in-ferolateral aspect of the ON and extends from the OphAentrance into the orbit to the point where the artery chang-es direction and becomes the second segment (Fig. 3A).The second segment crosses, in a lateral to medial direction,over (Type 1) or under (Type 2) the ON from the inferolat-eral to the superomedial aspect of the nerve. At this point,the OphA turns anteriorly. We found the OphA to cross the

ON superiorly in four specimens on both sides (57%). In theremaining three specimens (43%), the OphA crossed theON inferiorly on both sides. The point where the OphAcrosses the ON is easily identified on the lateral angiograph-ic projection (Fig. 4). The third segment of the OphA ex-tends from the angle where the second segment bends at themedial aspect of the ON to its termination at the superome-dial angle of the orbital opening (Fig. 3A).

The intraorbital OphA gives rise to several branches,which can be schematically classified into four groups: ocu-lar, orbital, extraorbital, and dural. The ocular group in-cludes the CRA and the ciliary arteries supplying the retinaand choroid. The orbital group includes the lacrimal andmuscular branches. The extraorbital group consists of thesupraorbital, anterior and posterior ethmoidal, palpebral,dorsal nasal, and supratrochlear arteries. The dural group in-cludes the two recurrent superficial and deep arteries. Theethmoidal and lacrimal branches of the OphA also con-tribute to the dural supply.

The order in which the OphA branches originate varies inrelation to whether the OphA crosses above (Type 1) orbelow (Type 2) the ON (Fig. 3). When the OphA crossesabove the ON, the first branch is the CRA and the second

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FIG. 2. Photographs showing the microanatomical features of the OphA and its intradural origin. A: The lateral walland roof of the left orbit and the intraorbital fat have been removed. After performing an anterior clinoidectomy, the oculo-motor (CN III), trochlear (CN IV), and ophthalmic (V1) nerves have been exposed by removing the dura of the lateral wallof the cavernous sinus. The ON is gently retracted to expose the origin of the left OphA. B: Enlarged view of panel A.The OphA arises at an acute angle from the superomedial aspect of the ophthalmic segment of the ICA just above the dis-tal dural ring. C: After its origin, the OphA courses anteriorly and laterally below the ON on the upper surface of the op-tic strut, and extends into the dural sheath of the ON on its inferolateral aspect to enter the optic canal. Intracranial perfo-rating branches directed to the ventral aspect of the ON (CN II) can arise from the OphA a few millimeters after its origin.CN = cranial nerve; Lat. = lateral; M. = muscle; Rec. = rectus; Seg. = segment.

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FIG. 3. Photographs showing the two primary patterns of the intraorbital course of the OphA. A: This posterosuperi-or view of the right orbit shows the Type 1 pattern of the intraorbital course of the OphA. The orbital roof and the lateralwall of the orbit have been removed and the intraorbital structures dissected. The superior rectus, the levator, and theoblique muscles have been retracted to expose the OphA. The part of the OphA as it extends into the orbit can be dividedinto three segments. In the Type 1 pattern, the OphA crosses over the ON, passing from the inferolateral to its superome-dial aspect. B: The ON is retracted medially, exposing the early intraorbital branches of the OphA. In Type 1 OphA, theCRA is usually the first branch of the OphA. In this specimen the CRA arises with the lateral posterior ciliary artery froma common trunk. C: Posterosuperior view of the right orbit in another specimen, showing the Type 2 pattern. The orbitalroof and the lateral wall of the orbit have been removed and the intraorbital structures dissected. The superior rectus mus-cle has been divided near the globe and retracted posteriorly to expose an OphA that courses below the optic nerve. D:The ON has been divided and retracted to expose the second segment of the OphA. In this pattern, the first branch is usu-ally the lateral posterior ciliary artery, whereas the CRA is the second branch. Cent. = central; Cil. = ciliary; Ethm. = eth-moidal; Med. = medial; Musc. = muscular; N. = nerve; Nasocil. = nasociliary; Obl. = oblique; Ret. = retinal.

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branch a posterior ciliary artery (lateral or medial); the thirdbranch is usually the lacrimal artery (Fig. 3A and B). Whenthe OphA crosses below the ON, the first branch is usuallythe lateral posterior ciliary artery and the second is the CRA(Fig. 3C and D).

In all specimens, the CRA arose from the first or secondpart of the OphA at the inferolateral aspect of the ON, medi-ally to the ciliary ganglion. Its diameter at the origin was amean of 0.2 mm (range 0.1–0.4 mm). In 43% of the orbits,the CRA arose directly from the OphA. In the remainingorbits, the CRA originated from a common trunk with theposterior ciliary and muscular branches (Fig. 3B). The CRApierced the lower medial aspect of the ON a mean of 10 mm(range 7–15 mm) behind the globe and reached the globethrough the center of the ON. In all orbits, the CRA was aterminal branch.

The number of posterior ciliary arteries ranged from twoto five, and in all orbits two long posterior ciliary arteries(one medial and the other lateral) were found. The long andshort posterior ciliary arteries course with the short and longposterior ciliary nerves and extend into the sclera close tothe ON to supply blood to the choroid.

The lacrimal artery typically courses with the lacrimalnerve superomedially to the lateral rectus to reach the lac-rimal gland (Fig. 5A). The diameter of the lacrimal arteryranges from 0.3 to 0.6 mm (mean 0.5 mm). In the mostcommon pattern of lacrimal gland vascularization (71% oforbits), the lacrimal artery arose as a separate branch fromthe main OphA trunk (Fig. 5A). In the remaining cases, thelacrimal artery arose from the MMA as a meningolacrimalartery (Fig. 5B). When a meningolacrimal artery was foundin our specimens, we did not observe any anastomosis ofthis vessel with the main OphA system. The lacrimal arterytypically has muscular, zygomatic, and glandular branches.Short ciliary arteries to the choroid can also originate fromthe lacrimal artery.

The anterior and posterior ethmoidal arteries supply

blood to the ethmoid sinuses, the nasal cavity, and the sep-tum. The anterior ethmoidal artery was detected in all orbitsas an independent branch of the OphA and was usually larg-er than the posterior ethmoidal artery. The diameter of theanterior ethmoidal artery at its origin ranged from 0.3 to1 mm (mean 0.6 mm). This artery courses medially andnormally below the superior oblique muscle, and extendstoward the anterior ethmoidal foramen. While crossingthe anterior ethmoidal foramen, this artery provides smallbranches to the ethmoidal air cells. Intracranially, the arterycourses between the two layers of the falx as the anteriorfalcine artery (also termed the anterior falx artery or arteryof falx cerebri), which provides variable branches to the du-ra of the anterior cranial fossa and anastomotic branches tothe posterior ethmoidal artery.

The posterior ethmoidal artery is an inconstant branch ofthe OphA and was detected in 50% of our orbits. This arterytypically arises as a defined branch from the OphA. Its di-ameter ranges from 0.3 to 0.8 mm (mean 0.4 mm). After itsorigin, the artery enters the posterior ethmoidal canal, pass-ing over or under the superior oblique muscle. Intracrani-ally, the posterior ethmoidal artery sends branches to the du-ra of the posterior and medial third of the anterior cranialfossa.

The supraorbital artery arises from the OphA in the sec-ond or third segment and exits the orbit through the su-praorbital foramen or through a supraorbital notch. Anasto-moses between the supraorbital artery and the vascular sys-tem of the superficial temporal artery are usually detectedalong the superior temporal line and form a potential sourceof collateral blood supply between the ECA and the ICAsystems.

The supratrochlear (or frontal) and dorsal nasal (or nasal)arteries are the terminal branches of the OphA. The su-pratrochlear artery leaves the orbit from the medial portionof the supraorbital ridge, is directed frontally, and has richanastomoses with the contralateral supratrochlear artery.The nasal artery pierces the orbital septum above the medi-al palpebral ligament, courses on the root of the nose in theopposite direction to the supratrochlear artery, and anas-tomoses with the ipsilateral angular artery, the terminalbranch of the facial artery, and the contralateral nasal arteryat the dorsum of the nose. A single anastomotic channel ora rich and tiny anastomotic network of small vessels canconnect the angular artery with the supratrochlear artery(Fig. 6).

The recurrent branches of the OphA, one superficial andthe other deep, usually course through the SOF and supplythe cavernous sinus dura and the tentorium.12 The deep re-current OphA arises from the initial intraorbital portion ofthe OphA, reaches the cavernous sinus coursing through thetendon of Zinn and the medial aspect of the SOF, and anas-tomoses with the inferolateral trunk of the intracavern-ous carotid artery. The superficial recurrent OphA can arisefrom OphA branches as well as directly from the intra-orbital OphA or the MMA. This recurrent branch passesbackward through the SOF or optic canal to reach the duraof the roof of the cavernous sinus and can continue caudal-ly as the marginal tentorial artery.

Middle Meningeal Artery Supply to the Orbit. The MMAsupply to the orbit presents two distinct patterns (Fig. 5).When the lacrimal artery originated from the OphA (in 10

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FIG. 4. Angiogram of a lateral view of the left common carot-id artery, showing the OphA and its main orbital and extraorbitalbranches. The second part of the OphA presents with a typical bay-onet appearance (between the arrowheads) as it crosses the ON ina lateral to medial direction. The “safety point” for embolization ofpathological processes supplied by the OphA is beyond the secondsegment of the OphA after the origin of the CRA. Supratroch. = su-pratrochlear.

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sides of our sample; 71%), we found that the frontal branchof the MMA, while running medially to the sphenoid ridge,provided a recurrent meningeal branch (Fig. 5A). Thisbranch courses in the narrow groove between the greaterand lesser wings (Fig. 1B) of the middle cranial fossa, pass-es through the apex of the SOF, and anastomoses with thelacrimal artery (a branch of the OphA) (Fig. 5A). Thisbranch originating from the MMA has been referred to asa recurrent meningeal branch, orbital branch, or sphenoid-al artery of the MMA. Its size has ranged from 0.2 to 0.4mm (mean 0.3 mm). The anastomosis between the recurrentmeningeal artery and the lacrimal artery is located in theapex of the SOF. The recurrent meningeal artery usuallyprovides small branches for the periorbita and for the dura,where the dura blends into the periorbita of the orbital apex.

In four sides (29%) of two specimens in our study, thefrontal branch of the MMA provided a meningolacrimalbranch, which coursed toward the Hyrtl canal to the lacrimalgland (Fig. 5B). The meningolacrimal artery at the end ofthe canal extends into the periorbita, accompanies the lacri-mal nerve, and courses over the upper aspect of the lateralrectus to reach the lacrimal gland (Fig. 5B). In such cases,we found that the vascularization of the lacrimal gland isprovided solely by the MMA through the meningolacrimalartery, without contributions from the OphA system. Themeningolacrimal artery, with an average diameter of 0.4

mm (range 0.3–0.5 mm), is also involved in the vasculariza-tion of the extraocular muscles, especially the lateral rectus.In two sides of one specimen (14%), the frontal branch ofthe MMA bifurcated into a meningolacrimal artery and asmaller recurrent meningeal branch, which enters the orbitthrough the SOF. This smaller recurrent branch providedsmall muscular vessels and an inferior ramus for the OphA,and in one of the two sides anastomosed with the branchesof the OphA.

Discussion

Anatomical Variations of the OphA and Their ClinicalSignificance

A thorough understanding of the microsurgical anatomyof the OphA, the appearance of its branches on angiograms,and its anastomoses with the ECA system are all necessaryto perform safe and effective endovascular and other surgi-cal procedures involving this critical vascular area. Severalanatomical anomalies of the origin of the OphA have beenreported. The OphA can originate extradurally from the cli-noidal segment or the intracavernous portion of the ICA in2 to 8% of cases.5,6,22,34 In such instances, the OphA––instead of entering the orbit through the optic canal––pass-es through the SOF or through an anomalous foramen in theoptic strut termed the ophthalmic foramen24 or double op-

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FIG. 5. Photographs showing the MMA blood supply to the orbit. A: Superior view of the left orbit. The orbital roofand the lateral wall of the orbit have been removed and the intraorbital structures dissected to show the anastomosis be-tween the lacrimal artery and the recurrent branch of the MMA. The recurrent meningeal branch of the MMA coursestoward the apex of the SOF where it establishes an anastomosis with the lacrimal artery. B: Superior view of the left orbitin another specimen. The orbit and the meningolacrimal canal have been unroofed and the orbital fat has been removed.The meningolacrimal artery courses toward the Hyrtl canal to enter the orbit and reach the lacrimal gland, where it is theonly blood supply for the gland. When the meningolacrimal artery is present, anastomoses between the OphA system andthe MMA may or may not be present. Div. = division; Front. = frontal; Lev. = levator; Ophth. = ophthalmic; Recur. = re-current.

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tic foramen.33 On rare occasions, a duplicate origin of theOphA from the ICA can be encountered.23 In these cases,the upper duplicate artery arises from the supraclinoid por-tion of the ICA and passes through the optic canal, whereasthe lower duplicate artery arises from the ICA in its intra-cavernous portion and passes through the SOF. Kyoshimaand colleagues11 reported two cases of an intradural originof the OphA in a series of patients with juxta–dural ring an-eurysms. During surgery for such an aneurysm, if the OphAis not observed intradurally, the surgeon should be remind-ed of the possible existence of this variation when section-ing the dural ring on the medial side.

The origin of the OphA from the MMA is a rare anom-aly.8,16,32 Hayreh and Dass8 described two cases in 170 ana-tomical specimens in which the only source of blood supplyto the orbit was the MMA. Watanabe and coworkers32 foundonly 21 reported cases of this anomaly in their review. AnOphA origin from the MMA has important microsurgicaland endovascular implications. Shima et al.29 reported onecase in which blindness occurred after a pterional cranioto-

my due to coagulation of an OphA arising from the MMA,while the dura was elevated in this region. Once an originof the OphA from the MMA is angiographically confirmedin lesions supplied by the MMA, an endovascular emboli-zation procedure carries the risk of visual impairment due toembolic occlusion of the CRA (if the microcatheter is notpositioned distally to the anomalous origin of the OphA, orif reflux of embolization material occurs during injection).

Anatomical Significance of the Ophthalmic Artery DuringNeuroendovascular Procedures

With continued advances in microcatheter and micro-guidewire technology, the OphA and its branches can be se-lectively catheterized and embolized to treat various vascu-lar and neoplastic processes involving the orbit and/or theanterior skull base.15 Vascular supply from the OphA can bedetected in intraorbital lesions such as meningiomas andarteriovenous malformations,27 as well as in extraorbitallesions such as meningiomas30 and ethmoidal dural arterio-venous fistulas.14 Use of superselective angiography andembolization have been reported in determining a diagnosisand treatment of the aforementioned pathologies and in themanagement of nonneurosurgical patients with lesions suchas epistaxis,4,17,20 facial arteriovenous malformations,2 andCRA occlusion.21

Several anatomical factors make endovascular approach-es to lesions supplied by the OphA challenging and poten-tially hazardous because of the risk of visual impairmentand blindness. The critical factor influencing the successfulembolization of lesions fed by the OphA or its branches isthe location of the CRA. In accordance with previous re-ports,8 our study data confirmed that the order in which theCRA arises from the OphA is related to whether the OphAcrosses above or below the ON. When the OphA passesover the ON, the CRA was invariably the first branch ofthe OphA and the posterior ciliary artery was usually thesecond branch. This pattern was reversed when the OphAcrossed under the ON. Embolization of pathological pro-cesses supplied by the OphA can be safely performed if theOphA can be superselectively catheterized past the “safetypoint.” This point occurs beyond the second segment of theOphA,1,19 after the origination of the CRA (which arisesfrom the first or second segment of the OphA).7 The partialregression of the arterial ring, which develops around theON during embryological development, indicates in the lat-eral angiographic projection the point at which emboliza-tion can be safely continued.1 When the CRA cannot beconclusively excluded from the region of embolization, aprovocative amytal/lidocaine test can be helpful in localiz-ing this critical vessel in relation to the catheter position.

Internal and External Carotid Artery Collateral PathwaysThrough the OphA

The ECA system forms a rich vascular network aroundthe orbit that is able to provide collateral flow to intracranialcirculation in the event of severe ICA stenosis or occlusion.The angular branch of the facial artery anastomoses withthe nasal artery, a terminal branch of the OphA. The distalbranches of the OphA (supraorbital, frontal, inferior, andlateral palpebral arteries) may also anastomose with branch-es of the superficial temporal artery. The infraorbital and the

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FIG. 6. Photograph of the anterior view of the medial portion ofthe left orbit. The skin around the orbit has been removed to exposethe anastomotic network between the supratrochlear artery (theterminal branch of the OphA) and the angular artery (the terminalbranch of the facial artery).

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anterior deep temporal arteries, which are branches of themaxillary artery, provide branches to the inferior lacrimalterritory13 to supply an additional potential source of collat-eralization. Reversal of flow through these extracranial–in-tracranial anastomotic channels can provide enough collat-eral flow to the visual system after surgical or endovascularocclusion of the origin of the OphA. Due to these preexist-ing anastomotic channels, the risk of vision loss after acuteocclusion of the OphA origin is relatively low (approx-imately 10%), with 90% of patients expected to remainasymptomatic.10 To test the adequacy of collateral supply tothe retina, the use of temporary balloon occlusion of theOphA and the ICA with synchronous visual acuity mea-surement has been suggested.28

Clinical Importance of Anastomoses Between the OphAand the MMA

Detailed knowledge of the anastomoses between theOphA and branches of the MMA is critical for avoiding dis-astrous complications (such as vision loss) during embo-lization of lesions fed by the MMA. Anastomoses betweenthe recurrent branch of the MMA and the lacrimal artery atthe apex of the SOF are commonly found in anatomicalspecimens. Hayreh and Dass8 found this anastomosis inall 59 specimens they studied. Similarly, Liu and Rhoton16

described this anastomotic connection in nine of 10 speci-mens. In our study, we found this anastomosis in all casesin which the lacrimal artery originated from the OphA (71%of sides). In 29% of sides we found the blood supply to thelacrimal gland to originate solely from the frontal branchof the MMA. In such cases, an anastomosis between theMMA system and the OphA system through a recurrentmeningeal branch was found in only 25% of cases. In allspecimens, anastomosis between the recurrent branch of theMMA and the OphA system was observed in 78% of orbits.When a true meningolacrimal artery is detected (a branchof the MMA providing the vascularization of the lacrimalgland without contributions from the OphA system), the re-current meningeal artery is usually smaller than in the otherpattern of MMA supply to the orbit. In such cases, this anas-tomosis is very thin and can be poorly injected or disruptedduring dissection, helping to explain the discrepancies be-tween the results of previous studies8,16 and those reportedhere. Anastomotic connections between the MMA and theOphA represent a potentially dangerous source of com-plication during endovascular procedures. Mames et al.17

reported vision loss in a patient after embolization of the in-ternal maxillary artery to control traumatic epistaxis. A cho-roidal blush was observed upon injection of 100 to 200 mmpolyvinyl alcohol particles into the internal maxillary arterybefore embolization, and although the injection was madebeyond the origin of the MMA, reflux caused particles toreach the OphA and the CRA through collateral pathways,and caused blindness. The anastomotic connections be-tween the OphA and MMA in patients with occlusion of theICA may allow for passage of retinal emboli in the presenceof atheromatous and/or ECA disease. Amaurosis fugax inpatients with ICA occlusion and atheromatous disease ofthe ECA have been described3 and explained on the basis ofthese and other anastomotic connections. Permanent visualloss, retinal infarction, and ophthalmoparesis have also beenreported after injection of dental anesthesia.25 The plausible

explanation for these results is an intraarterial injection ofthe anesthetic solution into the maxillary artery with back-flow into the MMA. The ocular symptoms result from thepassage of the solution injected into the CRA through therecurrent meningeal branch of the lacrimal artery. Monoc-ular blindness, reported to be as high as 1.8% of patientswith meningiomas following preoperative embolization ofMMA branches, can also be explained by the passage ofparticles through these anastomotic channels.26

Conclusions

With recent advances in endovascular procedures, thera-peutic embolization of vascular and neoplastic processes in-volving the area of the OphA are common. Detailed knowl-edge of the microsurgical anatomy of the OphA is critical toperforming safe and effective endovascular procedures. Inaddition, the common presence of anastomotic connectionsbetween the OphA and the MMA can be a source of dis-abling complications during embolization of lesions sup-plied by the MMA. Knowledge of these anastomoses andtheir frequency, pattern, and variance is crucial to minimiz-ing these problems.

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Manuscript received September 3, 2005.Accepted in final form August 7, 2006.Address reprint requests to: Giuseppe Lanzino, M.D., Department

of Neurosurgery, University of Illinois College of Medicine at Pe-oria, 530 Glen Oak Avenue, Peoria, Illinois 61637. email: [email protected].