Major Review

Vascular Malformations of the Orbit: Classification and the Role of Imaging in Diagnosis and Treatment Strategies* Jack Rootman, M.D.*†, Manraj K.S. Heran, M.D.‡, and Douglas A. Graeb, M.D.‡ *Department of Ophthalmology and Visual Sciences, †Department of Pathology and Laboratory Medicine, and ‡Department of Radiology, University of British Columbia and the Vancouver General Hospital, Vancouver, British Columbia, Canada

Purpose: To describe the authors’ experience with orbital vascular malformations using the International Society for the Study of Vascular Anomalies (ISSVA) classification and the preferred radiologic techniques. Methods: Review of clinical and radiologic experience from 1976 to 2012. This article presents the findings from several studies conducted on vascular malformations of the orbit, all of which received institutional review board approval when needed. Results: The orbital vascular malformations can be evaluated, classified, and managed according to the ISSVA classification to provide a common language of communication between specialties, which takes into account flow dynamics. Conclusions: The ISSVA can be applied for vascular malformations of the orbit. (Ophthal Plast Reconstr Surg 2014;30:91–104)

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he management strategies for high- and low-flow orbital vascular malformations require an understanding of pathogenesis, classification, evaluation, and specific hemodynamics. In the last 3 decades, our knowledge has changed dramatically based on the development of more refined investigations and the work of specialized clinics and societies devoted to the study and management of these complex disorders. Our thinking has evolved over 35 years from a cooperative involvement of specialists in clinical evaluation, static and dynamic imaging, surgery, vascular intervention, and pathology of over 350 cases. These lesions are best understood by considering angiogenesis, phenotypic types, and especially hemodynamics. Management strategies should be based on these factors.

ANGIOGENESIS Malformations can occur at any point during the developmental sequence of the vascular system, including the arterial, venous, or lymphatic vessels, and can consist of these elements alone or in combination.1–3 Vascular malformations of the head and orbit are derived from the vessels of the brain and therefore, not infrequently, have intracranial vascular and structural

*See also p.180. Accepted for publication December 2, 2013. The authors have no financial or conflicts of interest to disclose. This article is based on the study by Rootman et al.21 Address correspondence and reprint requests to Jack Rootman, M.D., Department of Ophthalmology, University of British Columbia, 2550 Willow Street, Vancouver, BC V5Z 3N9, Canada. E-mail: [email protected] DOI: 10.1097/IOP.0000000000000122

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components.4–6 They may also be part of a systemic diathesis, which will not be discussed here.7,8

CLASSIFICATION The Table outlines this current approach to classification in the orbit based on the International Society for the Study of Vascular Anomalies (ISSVA) classification of nonorbital vascular anomalies, which has expanded upon Mulliken and Glowaki’s classification based on pathologic features.9–15 It also reflects the hemodynamic categories of high-flow and low-flow lesions and their phenotypic subtypes.16–18 There are transitional lesions that have elements of more than 1 type depending on where in the developmental sequence they occur. High-flow lesions include arteriovenous malformation (AVM) and congenital arteriovenous fistulas (AVF). Low-flow lesions are divided into venous malformations (VMs), lymphatic malformations (LMs), and combined lymphaticovenous malformations (LVMs). Pure VMs include distensible and nondistensible lesions. Pure LMs can be macrocystic, microcystic, and mixed macrocystic/microcystic, all of which may have solid stromal components. The combined LVMs include 2 types based on hemodynamics. The venous dominant (VD-LVM distensible) has a significant venous element that may demonstrate distensibility on clinical examination (a positive Valsalva response) and/or during dynamic investigations, including dynamic arterial and Valsalva-augmented venous phase multidetector CT angiography (DP-MDCTA) described by Heran et al.19 (see accompanying article, p. 180, this issue), MRI, ultrasound with Doppler assessment, or on direct injection with and without Valsalva maneuver. The lymphatic-dominant malformation (LD-LVM) has a less evident, or minimal, venous component and is a nondistensible lesion. In terms of location, malformations can be anterior (superficial), deep (retrobulbar), combined (with anterior and deep components), or complex where they extend outside the orbit into adjacent tissues (Fig. 1).20

HEMODYNAMICS It is important to consider the hemodynamic effect of size and type of inflow and outflow channels and those within the lesion in each category.22 The effects on flow are like plumbing systems, where dynamics may differ depending on inflow or outflow channel size (large, small) and type (normal, dysmorphic) and the number (many, few) of connections. It is worthwhile to consider these aspects (inflow–outflow) within the 2 principle flow categories (high flow versus low flow), regardless of the dominant phenotype (arteriovenous, venous, lymphatic, or combined). Differing hemodynamics may be clinically evident as pulsation in high-flow (arteriovenous) malformations, which vary according to nidus size and inflow–outflow characteristics.

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channels.23 Clinically, these distend and/or deflate slowly, a factor that can help in their management. With indirect or direct real-time dynamic studies, these fill and empty slowly. In the combined lymphaticovenous category, the range includes those with large outflow and numerous venous channels (VD-LVM) to those that are LD and have minimal (microscopic) venous components, which do not distend and show little or no evidence of outflow even on direct injection (LD-LVM; see “Lymphatic Malformations”).

Classification of congenital vascular malformations (phenotypes) High flow  Arterial aneurysm  Arteriovenous fistula  Arteriovenous malformation Low flow  Simple   Venous malformation     Distensible*     Nondistensible      Cavernous venous malformation    Lymphatic malformation     Macrocystic     Microcystic (diffuse/microscopic)     Mixed (macrocystic/microcystic)  Combined†    Lymphaticovenous malformation     Venous dominant     Lymphatic dominant

ASSESSMENT OF FLOW The major ways the authors assess flow are:

*Some or all of a VM may have distensible components on Valsalva maneuver. †Combined malformations may be composed of any combination of distensible or nondistensible venous components and any subtype of LM (macrocystic/microcystic/mixed).

However, in the case of VMs and LVMs, the character of outflow channels is the dominant hemodynamic consideration. The outflow effect of a distensible VM or LVM with significant connection to the systemic venous circulation is demonstrated when venous pressure is raised (Valsalva maneuver) by development of profound and rapid proptosis and/or displacement (distension) followed by relatively fast deflation on relaxation (generally, over a few seconds). Typically on systemic contrast injection (DP-MDCTA with and without Valsalva maneuver) or on direct lesional injection, these varices fill and empty quickly if they have large outflow channels. In contrast, another hemodynamic is distensible VMs with narrower and/or fewer outflow

1. Clinical Valsalva, which is best performed by having the seated patient bend at the waist into a head-down position to increase abdominal pressure while performing the maneuver. The speed and degree of development of proptosis and/or globe displacement should be recorded either by direct timing or on video. Slow filling or deflation of lesions reflects a malformation with small channels and/or small outflow channels, whereas rapid filling and deflation reflects primarily large outflow vessels (Figs. 1 and 3 in accompanying article). 2. Assessment with Doppler ultrasound when available, with and without Valsalva maneuver. 3. CTA (DP-MDCTA), with Valsalva maneuver during the venous phase, is a very effective way of visualizing and characterizing the primary lesion(s) in the orbit and adjacent structures. It also determines the effect of distension on the orbital structures and flow in the lesion over time. It is critical to confirm a successful Valsalva maneuver by noting enlargement of the superior ophthalmic vein during the Valsalva phase compared with the earlier phase (see accompanying article). 4. Standard MRI with contrast, which can also be augmented by viewing the lesion during Valsalva maneuver or with the head in a recumbent position to promote backflow. Dynamic contrast-enhanced MR angiography (MRA) may

FIG. 1.  Left, Locations of orbital vascular malformations: superficial (yellow), deep (blue), and combined (red). The superficial lesions are limited primarily to the eyelid and conjunctiva. Deep lesions are retro- and peribulbar. Combined lesions are both superficial and deep. Complex vascular malformations may extend beyond the orbit to cranial, sinus, and facial distributions and may be multisystem (middle, right). The axial drawing (middle) shows extension of lesions into the temporalis and middle cranial fossa and the ethmoid sinuses. Reprinted with permission from Rootman et al.21

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potentially be used to evaluate the response to Valsalva.24,25 However, this technique currently does not provide the same level of relevant dynamic detail as ­DP-MDCTA because of the long acquisition times necessary for MRI and the decreased spatial resolution. 5. Direct injection of contrast into the malformation or via its feeding vessels, with digital image recording, assesses characteristics of the lesion and can be augmented with Valsalva during injection. This allows for mapping and planning of treatment by either gluing or excision26 or in performing sclerotherapy.27,28 6. Retrograde access through the venous system, which can also be used to reach and evaluate the malformation. Rarely, this may also provide an avenue for therapy and potential placement of thrombogenic coils into the lesion, although

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recanalization is not uncommon and the induced acute thrombosis can be very painful for several weeks.

HIGH-FLOW MALFORMATIONS Arterial Malformations. Arteriovenous Malformations. Arteriovenous malformations (AVM) are characterized by rapid arterial flow through the nidus into the draining venous circulation (i.e., arteriovenous shunting) (Fig. 2). They tend to occur in the choke anastomotic zones4 linking the angiosomes and can be intraorbital, where they have localized signs, transorbital, or periorbital and supplied by orbital vessels, where they can act to steal or shunt blood from the orbit leading to ischemic changes.29,30 They may cause pulsatile proptosis. Their altered flow patterns can lead

FIG. 2.  A, Drawing depicts an arteriovenous malformation (AVM) with arterial flow originating from the ophthalmic artery and venous flow through the superior ophthalmic vein to the cavernous sinus and the angular veins to the face. B, An arteriogram of a patient with an AVM demonstrates a large ophthalmic artery (thick arrow) with outflow to the superior ophthalmic vein (thin arrow). Reprinted with permission from Rootman et al.8

FIG. 3.  This young man had an inferior orbital and subcutaneous mass due to an underlying arteriovenous malformation (AVM) causing an intermittent steal syndrome. A, It is shown as a tangle of vessels on the early phase CT angiography. Selective angiography demonstrates inflow from branches of the ophthalmic artery (B) and from a maxillary branch of the external carotid artery (C), with rapid outflow through the facial vein. The authors did a selective embolization with glue through the maxillary branch (D and E) and the next day, removed the nidus with minimal bleeding (F), with a good postoperative result. Reprinted with permission from Rootman et al.21

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to venous stenosis, thrombosis, and/or hemorrhage.31 An orbital AVM may cause discomfort or pain when at rest or distended by Valsalva maneuver or may manifest pulsation, acute swelling (due to thrombosis), or hemorrhage resulting in ecchymosis.32 AVMs gradually enlarge with time as they recruit more arterial feeders. Routine CT shows diffuse enhancement because the contrast study is usually captured in the late phase when the lesion enhances almost uniformly. On the contrary, a distinct tangle of vessels is seen during the early phase of DP-MDCTA (Fig. 3A; Fig. 6 in accompanying article). MRI may have flow voids, while MRA shows enhancement of the nidus. Doppler ultrasound shows rapid flow with pulsation. On direct contrast injection (selective angiography) of an orbital AVM, blood flows through the ophthalmic artery or a tributary into the lesion and quickly out through the efferent venous system (Figs. 3B,C).21 In the experience of the authors, orbital lesions often have supply from the external carotid circulation as well and are best characterized by formal catheter angiography after initial noninvasive diagnostic imaging has been performed. Treatment Strategies. Understanding the hemodynamics allows for appropriate management strategies. They can be observed, but the nidus tends to enlarge, recruiting vessels over time and may become painful when straining or following a thrombosis or hemorrhage. AVMs can also demonstrate ­high-flow arteriopathy of the inflow (nidal) arteries, with potential flow-related aneurysms or with similar changes occurring on the venous side as well. The authors have seen such an instance where the supply vessel (ophthalmic artery) narrowed over time due to high flow–related stromal hyperplasia preventing successful cannulation. Although AVMs may be excised surgically, the margin is often relatively poorly defined in the soft tissues, and component vessels may be difficult to identify with a risk of significant bleeding and surgical morbidity during direct resection. The best method of management is a combined approach of preoperative selective angiography with embolization followed by resection of the nidus (Fig. 3D–F).22,33,34 Failure to resect the nidus completely typically leads to AVM recurrence. In some instances when unable to selectively intervene endovascularly, the inflow vessels can be clipped intraoperatively prior to resection of the nidus to reduce flow. Additional or adjunctive measures include alcohol sclerotherapy, direct intralesional injection, and laser treatments. The goal should be elimination of the nidus; however, this may not be possible with all AVMs without significant morbidity, local tissue damage, or functional injury.

nondistensible category is cavernous VM ­(so-called “cavernous hemangioma”). Distensible VMs. Distensible VMs have significant communication with the venous system through normal or dysmorphic channels. Clinically, these may expand with Valsalva maneuver and decompress at variable rates depending on inflow and, primarily, outflow dynamics. They may present with painful bouts of spontaneous thrombosis22,37,38 and/or can have bleeds. The authors have noted 3 lesional types of VMs in the orbit: dysmorphic, spongy, and cavitary.14,15 In terms of intraorbital frequency, in the experience of the authors, they are dominantly dysmorphic, followed by spongy, and less frequently cavitary (Figs. 4 and 5). In addition, these distensible VMs are associated with different outflow channels that affect clinical physiology, as in a case of a dysmorphic lesion with outflow to normal superior ophthalmic vein (Fig. 5, left). Alternatively, there may be dysplastic venous outflow (Fig. 5, middle). Finally, there are VMs that distend and deflate slowly during and following Valsalva maneuver and on direct venography or lesional cannulation, with little or restricted outflow (Fig. 5, right).

Aneurysms. Arterial aneurysms are rare in the orbit and are usually nonsymptomatic but may require intervention. Most can be handled by endovascular interventional methods. Some cases may require combined endovascular and surgical management or exclusively surgical management.35,36 Arterial Dysplasias. The orbit can be involved as part of systemic or cerebral vascular malformations and collagen vascular syndromes, such as Marfan and Ehlers–Danlos. Management is usually the domain of specialized vascular teams but may, on occasion, require some orbital interventions.

LOW-FLOW MALFORMATIONS Simple. Venous Malformation. Orbital VMs can behave as distensible or nondistensible lesions (Table). The most common lesion in the

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FIG. 4.  Three types of venous malformations: dysmorphic (top), spongy (middle), and cavitary (bottom). Reprinted with permission from Legiehn and Heran.15

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FIG. 5.  The intraoperative venography demonstrating outflow characteristics of venous malformations. Direct injection of a dysmorphic tangle with outflow through the normal superior ophthalmic vein (left). In contrast, the middle image demonstrates a dysmorphic nidus with dysplastic outflow. Finally, the right image shows a spongy lesion with minimal outflow following direct injection. Top-left, Reprinted with permission from Lacey et al.26. Top-middle and top-right, Reprinted with permission from Rootman et al.21. Drawings adapted with permission from Legiehn and Heran.15

FIG. 6. Axial CT angiography (CTA) scans of a cavitary venous malformation pre- (A) and post-Valsalva (B) maneuver. Note expansion and almost complete enhancement post-Valsalva and the typical tapering of the posterior margin toward the apex. Coronal CTA scans pre- (C) and post-Valsalva (D). Note significant enlargement of the lesion post-Valsalva with displacement of adjacent structures. Also note that the superior ophthalmic vein (D, arrow) has dilated during Valsalva. Reprinted with permission from Rootman et al.21

On clinical examination, about 60% of the distensible VMs have a detectable positive Valsalva maneuver. The remaining 40% may not demonstrate clinical distention but show distension on appropriate imaging. This would include arterial and Valsalva-augmented venous phase CTA and/or direct cannulation and phlebography at the time of surgical resection, first without and then with intraoperative Valsalva maneuver (induced by the anesthesiologist raising intrathoracic pressure).

In the past, contrast studies that were performed with direct coronal/head-down images were also able to demonstrate their distensible nature. Distensible VMs have been encountered that may become acutely painful if they undergo thrombosis or hemorrhage or even on sudden dilatation associated with physical stress37,39 (Fig. 2 in accompanying article). Patients with very large distensible malformations may become enophthalmic due to the gradual enlargement of the

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bony orbit and associated fat atrophy over time. They typically have an easily demonstrated proptosis or globe displacement on Valsalva maneuver. Distensible lesions may be painful on expansion, especially in young people or when lying prone (Fig. 1 in accompanying article). Spontaneous thrombosis is characterized by sudden painful expansion with tissue swelling. This episode will generally resolve over time without intervention, but recanalization can occur (Fig. 2 in accompanying article). On dual-phase CTA, distensible VMs demonstrate progressive filling (Fig. 6A,C), expand on Valsalva maneuver or with direct coronal scanning, and may not be detectable until a Valsalva maneuver is performed (Fig. 6B,D). The authors find dynamic CTA with venous phase Valsalva maneuver is very useful because the arterial non-Valsalva phase shows the initial smaller area of filling, with progressive filling of the lesion on the venous phase, while confirming expansibility and patterns of the malformations. Phleboliths are a common feature reflecting resolution of previous thrombosis. It is also worth noting that there may be more than 1 lesion in the orbit and they may not be connected (Fig. 1 in accompanying article). For instance, Figure 7 on direct venography shows an anterior-superior malformation with superior ophthalmic vein outflow and a second lesion, which is inferior and only appeared on the direct coronal scan or Valsalva. Retrograde jugular injections had been used in the past to help identify and characterize these lesions, although this is now rarely required. Direct injection of an orbital VM demonstrates the type of outflow pattern, a feature that can aid in management strategy.23,40 Hemorrhage from a malformation can be readily identified and can be followed clinically if there are no functional indications for intervention (Fig. 8A,B). On the contrary, an intralesional thrombus may take a long time to resolve. They have characteristic features of peripheral enhancement (due to flow around the edges of the clot or the phlebitis accompanying the thrombosis or both) (Fig. 8C,D). The underlying VM in patients presenting with thrombosis usually require observation only; however, they may recanalize and then require treatment (Fig. 2 in accompanying article). Acute intervention is reserved for those with significant pain, swelling, or clinical dysfunction. It should be noted that because vascular malformations occur as part of the abnormal development of the venous and lymphatic system of the head, they can be associated with intracranial developmental venous anomalies (DVA), which are usually incidental findings and are of little clinical significance. These DVAs can, however, be associated with cavernous VMs of the brain, which have a low risk of hemorrhage. The presence of an associated cavernous VM can be ruled out with dedicated MRI. The authors have encountered 2 cases of LVMs that had intracranial hemorrhage due to small periventricular cavernous VM.5 Treatment strategies. Distensible venous lesions can be observed, which the authors believe is appropriate in many instances.41 Indications for intervention include: persistent, untenable pain; functional deficit; acute thrombosis with severe pain; cosmesis; severe enophthalmos; and tense hemorrhage. Some lesions, if superficial, can be managed by intraoperative clipping, cautery and excision,42 or sclerosis. Because they are diaphanous, thin-walled, and are often more extensive than anticipated, there is a real risk of rupture and problematic operative bleeding. They may be handled more safely by direct operative mapping and glue embolization, followed by surgical excision,26 which is the operative technique the authors prefer.43 They are exposed and cannulated under direct vision intraoperatively or may be accessed percutaneously directly or using image guidance (such as ultrasound). Intralesional phlebography allows

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characterization of the extent and structure of the malformation and associated venous outflow. Glue embolization can be performed at the same time, with occasional requirement for compression of the outflow venous circulation to ensure optimal embolization. Ideally, the entire lesion can be filled in this manner, including the outflow venous channels, which may be difficult to manage surgically (Fig. 1B in accompanying article), before removal. Coils have been used to thrombose lesions but are associated with an extended period of painful orbital swelling following the procedure and may ultimately recanalize44,45 (Fig. 2 in accompanying article). The authors have tended to use traditional sclerosants, such as medical grade alcohol and 3% sodium tetradecyl sulfate, primarily for lesions outside the orbit because they may develop a posttreatment inflammatory reaction and swelling, which, if used intraorbitally, can cause complications associated with elevated orbital pressures due to the confined space of the orbit. The use of more gentle sclerosants (such as bleomycin A5 and doxycycline) diffused into the lesion

FIG. 7.  A, A distensible dysmorphic venous malformation of the eyelid and anterior orbit is easily seen on direct venography during Valsalva (B) with outflow through the superior ophthalmic vein. Postcontrast direct coronal CT of the same patient in a head-down position (C) shows a second distensible venous malformation in the posterior inferior orbit. A, Reprinted with permission from Rootman et al.21. B and C, Reprinted with permission from Rootman et al.8

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FIG. 8.  A, Contrast-enhanced CT scan of a patient who presented with acute painful proptosis and hemorrhage due to an intralesional thrombosis, which settled rapidly. B, Gadolinium-enhanced MRI of the same patient performed weeks later show only a tiny residual venous malformation. C, Contrast-enhanced axial CT scan of a patient presenting with a painful proptosis that developed over several days. Note the denser rim of this lesion, which is characteristic of a thrombosed varix. D, A scan with contrast performed 1 month later shows shrinkage of the lesion after observation alone. Reprinted with permission from Rootman et al.21

may allow for percutaneous treatment of lesions and can be used in combination with outflow obstruction when needed.27,28,46,47 Nondistensible VMs. True nondistensible VMs (with the exception of small distensible lesions that are not clinically detected easily but are visible with appropriate investigation) are, in fact, quite rare. The clinical profile for these lesions is typically presentation of spontaneous and rapidly progressive proptosis due to hemorrhage; in some instances, this presentation is anteceded by mild proptosis. On imaging, the lesion appears as a cystic mass due to the formation of a pseudocapsule. On contrast injection, the capsule may enhance in part or completely. At surgery, the hemorrhagic cyst when exposed and dissected typically has a thin mass of fine vessels on the surface of the capsule, which may enhance on direct injection of contrast into the lesion and also appear histologically.8,48 On occasion, the authors have noted a network of small dysplastic vessels with venography. Cavernous VMs. The authors wish to emphasize that ­so-called “cavernous hemangiomas” are not tumors but are VMs.49–51 Histologically, they have noted that orbital cavernous VMs are similar to those in the liver and subcutaneous tissues,49,50 where they also commonly occur.52 The hemodynamics consist of focal filling in the early phase of contrast injection, reflecting their vascular pedicle,

and progressive filling in the venous phase imaging, suggesting modest to minimal communication with inflow and outflow channels (Fig. 9, top).53 Further, there is evidence histologically and histochemically of thrombosis and neovascularization with stromal hyperplasia leading to slow but progressive expansion over years.48,54 Having recognized their relative vascular isolation, the authors and others55 have managed many by puncturing them intraoperatively, shrinking the mass by exsanguination, and then removing the smaller lesion (through conjunctival or skin incision) usually without a marginotomy or lateral orbitotomy. These malformations (as is the case with other vascular malformations) can sometimes be multifocal.56 The authors have also noted that patients with distensible spongy VMs and small outflow–inflow channels have patchy, slow filling of lesions in the early phase of CTA, more filling in the late phase, and positive Valsalva due to low inflow–outflow. They are very similar in appearance on CTA to cavernous VM except that there is modest, often slow distensibility clinically, a persistent mass effect, and slow expansion on Valsalva during late phase CTA. However, besides distensibility, they also have a different morphologic configuration, with a narrowing or indistinct posterior margin versus the normally rounded posterior margin of a cavernous VM and may have visible outflow on direct lesional contrast injection (Fig. 9).23,26

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FIG. 9.  CT angiogram with contrast in the early phase of a cavernous venous malformation (upper left) and a spongy varix (lower left) demonstrates minimal and spotty enhancement. In the late phase with Valsalva maneuver, the enhancement has spread to involve more but not the entire lesion, which expanded only minimally in the case of the spongy varix (lower right) and not at all in the cavernous lesion (lower left). Note the relationship of the cavernous venous malformation to the ophthalmic artery (arrows). Reprinted with permission from Rootman et al.21

FIG. 10.  This 7-year-old boy had a diffuse microcystic anterior lymphatic malformation affecting his upper eyelid and brow. The contrast MRI shows the lesion at age 15 years, just prior to direct excision through a eyelid crease incision. Reprinted with permission from Rootman et al.21

Treatment strategies. The indications for removal are significant progressive proptosis, compression of the optic nerve, hyperopia caused by posterior pole indentation, and sometimes

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FIG. 11. A 69-year-old woman had gradual onset of left proptosis that had been present for 7 years, evidence of left optic neuropathy. A, Left, CT revealed a well delineated, diffusely enhancing intraconal mass with evidence of orbital expansion. Right, T1-weighted MRI with contrast demonstrated a circumscribed mass, which displays heterogeneous enhancement. She underwent surgical excision. During excision, the margins of the lesion were noted to be well defined, and the mass clinically had a gross resemblance to a cavernous venous malformation. However, at the apex, it tapered and was firmly attached. It was carefully transected with little bleeding. Histologically, it was dominantly lymphatic (microcystic type) with fewer small venous channels. Some channels contained neovascular tufts, which accounted for the hemorrhage within the malformation (B, large arrow). In addition, there were multiple hemorrhages within the stroma (B, small arrows). Reprinted with permission from Rootman et al.21

persistent pain. Small lesions without functional effects can be observed. The authors have never seen patients present with sudden changes, hemorrhage, or evidence of calcification in histologically confirmed cavernous VMs. If so, the lesion is likely a LVM and highly unlikely to be a cavernous VM. They occur anywhere in the orbit. When in the apex, they can cause compressive optic neuropathy and may extend from or into the cavernous sinus or the optic canal.57 They have a capsule, are well defined, and can have intimate relationships to arteries or nerves, which may be incorporated into the capsule. Preoperative assessment with dynamic CTA can define in the arterial phase their relationships to vessels (Fig. 9). When located in the mid to anterior orbit, removal is relatively simple and performed without marginotomy. One of the authors’ (J.R.) preferred surgical approach is to enter the orbit nearest the lesion, expose the capsule, and gradually define the

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anterior one half to two thirds. A suture may then be passed through the core of the lesion, and pressure applied to promote exsanguination and reduce its size. Some surgeons recommend simple puncture and exsanguination using a needle and syringe. The mass is then rocked to expose the deeper surface plane for dissection aided by anterior traction on the suture. A second and rarely a third suture is placed in a deeper plane and the posterior border is carefully dissected free while rolling it out. Another method is to use a cryoprobe to rotate the tumor during dissection.58,59 If the lesion appears to be stuck, there is the possibility that it is a LVM (LD), which would necessitate reexamination of the imaging. Cavernous VMs are rounded at the posterior margins (Fig. 9, top), and LVMs are tapered and slightly irregular posteriorly.60 For LVMs or for “stuck” lesions, it is acceptable to truncate the posterior part and either leave a portion or carefully remove more of it piecemeal.16 For deep lesions, particularly within the annulus, the approach usually includes a marginotomy or even extended posterolateral bone removal (or rarely craniotomy) to more clearly access the lesion. Also, for deeper lesions approached directly, small-cupped forceps are useful to grip and manipulate the mass. Apical lesions that cause optic neuropathy are risky to remove and require skill and patience to avoid visual damage. It may be useful to incise the annulus to open the space or consider piecemeal removal for a lesion that is tight in the apex. Partial or piecemeal removal also applies to lesions where incorporation of a vessel in the capsule is identified.11 Finally, it should be noted that cavernous VMs that are very difficult to access might be treated with conformal radiotherapy (not radiosurgery).57 Surgical management of these lesions can be associated with significant complications if they are apical (such as vascular injury and associated ischemic- or traumatic-based vision compromise) or other complications if one enters the cavernous sinus. The authors do not prefer radiosurgery because risk of optic nerve damage is greater due to concentrated dosing. Finally, sclerotherapy may be a possible future treatment option for cavernous VMs, but its use for lesions in the annulus may risk swelling and pressure injury. Lymphatic Malformations. The orbit represents a somewhat unique site about lymphatic lesions because, with the exception of the skin, conjunctiva, lacrimal gland, and the perineural area,61 it does not normally have significant lymphatics throughout. Lymphatic malformations of the orbit (so-called “lymphangiomas”) are a type of low-flow malformation with a spectrum ranging from purely lymphatic to combined lymphatic VMs.62–64 The majority seen by the authors demonstrated mixed vascular elements histologically with varying degrees of dominance of lymphatic versus venous tissue. Histologically, they are made up of lymphatic and venous channels with stroma that may have dense lymphoproliferative, smooth muscle, fibrotic, and hemorrhagic constituents.65 They also have evidence of lymphaticovenous constituents on imaging when studied with and without contrast and Valsalva maneuver. Structurally, the ISSVA classification divides them into microcystic, macrocystic, and mixed lesions. The authors also categorize them dynamically into LVMs, either LD or VD. Purely, LMs of the orbit are relatively uncommon as most are mixed (i.e., lymphaticovenous), having a variable venous component. The clinical experience has been that pure LMs can be seen as isolated, often irregular masses, mostly located anteriorly (Fig. 10). Less often, they can appear as single or sometimes septated macrocysts. Microcystic LMs of the Orbit.The solid (microcystic) lymphangioma typically involves the anterior orbital structures and causes a soft, diffuse, and irregular thickening of the eyelid,

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FIG. 12.  A, Arterial phase imaging from a dual-phase contrastenhanced CT angiogram of the orbit without Valsalva maneuver demonstrates an extensive, irregular lesion of the orbit in a child. The lesion extends from the anterior to posterior limits. There are 2 focal areas of calcification, which represent phleboliths and the small area of contrast puddling in its posterior component, adjacent to and extending into the widened superior orbital fissure. B, Valsalva-augmented venous phase imaging from dual-phase contrast-enhanced CT angiography demonstrates an enlarged enhancing component posteriorly extending through the superior orbital fissure, representing a varix in a histologically proven distensible lymphaticovenous malformation. The lymphatic component was anterior where it shows irregular enhancement. The patient was treated with combined gluing, mapping, and excision. Reprinted with permission from Rootman et al.21

conjunctiva, and/or the anterior orbit. On slit lamp examination, they appear slightly xanthochromic with microscopic cysts, sometimes with clear lymphatic vessel-like elements. Occasional menisci are seen in the cysts, and the borders are ill defined. When the eyelid is involved, the subcutaneous tissues are thickened and soft, with occasional microscopic cysts noted at the eyelid margins. On imaging, these lesions appear as solid masses with irregular margins. The treatment strategy, usually for cosmetic reasons, is to excise them. Sometimes CO2 laser can be used to aid in excision and ablation. Direct excision is usually bloodless but frustrating because the margins are hard to define, and the surface is often involved. On occasion, the authors have completely excised the visible component and performed conjunctival or skin grafts to improve cosmesis

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(Fig. 10). Sclerotherapy for microcystic lesions has been less effective than for the macrocystic lesions.66 Microcystic LMs can also present clinically in the retrobulbar orbit, typically with slow proptosis. Although most present in the pediatric population, in some instances, they can present later in an adult (Fig. 11). These lesions are typically defined anteriorly but are irregular posteriorly, extending as a tail into the apex. At surgery, as mentioned, they can be mistaken for a cavernous VM but are more adherent, especially

posteriorly where they require sharper dissection. If they extend into the apex where complete excision might risk functional damage, they can be truncated because they bleed very little due to their lymphatic predominance.60 Sclerotherapy is also an option to reduce the size of these lesions when in the retrobulbar orbit. Macrocystic.Macrocystic LMs of the orbit may appear as isolated or few thin-walled cysts with variable T1 and T2 signal pattern on MR imaging, depending on the contents of

FIG. 13.  A, This 37-year-old woman had a 3-year history of progressive prominence of the right eye and a superomedial mass. On first examination, she had a mildly distensible lesion on Valsalva maneuver, which over a 3-month period became larger and more painful. There was a hypoattenuating multinodular anterior component and a rim-enhancing posterolateral component representing a venous varix (B, arrow). The authors treated this by exposing and removing the anterior solid component and cannulating the thrombosed (dysplastic) outflow varix. Digital subtraction injection within the lesion demonstrated flow around the thrombus (C) with this posterior component subsequently glue embolized (D). Histology demonstrates the large dysmorphic embolized vein (E, black arrow) adjacent to the more solid lymphatic component (E, white arrow) that contained many lymphorrhages and collapsed thin-walled lymphatic channels, which stained positively for D2-40 (which identifies lymphatics endothelium). She had no recurrence with 6 years of follow up. Reprinted with permission from Rootman et al.21

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the cysts. Sudden worsening of proptosis is often due to intralesional hemorrhage, related to the development of capillary tufts from the cyst walls, which is thought to occur in response to the increasingly proteinaceous fluid content and/or from stromal hemorrhage. The treatment strategy for isolated macrocystic LMs is conservative, with observation preferred if possible. When intervention is necessary, 3 options exist: 1) simple drainage, which is usually followed by slow transudative reformation of the cyst; 2) drainage followed by immediate sclerotherapy, which can be quite effective28; and 3) excision, which may be difficult because of the thin wall of the cyst. Excision can be aided by intraoperative drainage or filling with n-butyl cyanoacrylate or fibrin glue to aid excision.67 Mixed (Macrocystic/Microcystic). Mixed macrocystic/ microcystic LMs usually have a more solid-looking component and microcysts and macrocysts, with some evidence of a venous component. They typically present with slow proptosis; sudden worsening may occur as a result of intralesional hemorrhage. Most, when in the orbit, are combined LVMs, either LD or VD. Combined Low-Flow Malformations. Venous-Dominant LVMs. As noted, combined LVMs are on a clinical and imaging spectrum based on the dominance, size, and location of the venous or lymphatic components. The venous components typically are in the mid and posterior orbit. Generally, there are 2 types: those that are distensible clinically or on dynamic imaging (low flow; Fig. 12) reflecting a significant venous component and those that are not distensible (i.e., dominated by the lymphatic component classically referred to as “lymphangiomas”). About half of the patients with LVMs had a significant venous component (low flow). The majority in this category of VD-LVM had an earlier presentation (mean age, 6 years) with more frequent and more severe hemorrhages than the LD-LVM, which tend to present later (average, 13 years). When the VD lesions manifest later, they may present with evidence of

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thrombosis (Fig. 13; Fig. 4 in accompanying article). When they are complex and extend beyond the eyelid to involve the face, patients typically also have lesions in the mouth and cheek. If entirely within the orbit, they are local, and the authors have not noted associated oral lesions. Thus, if a child presents with a lesion that extends onto and beyond the eyelid, the cheek should be carefully examined for symmetry, and the roof of the mouth inspected because malformations in these areas are common. When they extend beyond the orbit, these components should be confirmed with CTA or contrast-enhanced MRI with particular attention to the cheek and pterygopalatine fossa. If lesions are present, the family/patient should be counseled regarding the potential for symptomatic presentation involving these areas. All of the VD-LVMs with a distensible venous component extended to include the mid or deep orbit, whereas most of the LD lesions had primary or significant anterior components. It is therefore important to suspect the presence of a venous component in deep lesions particularly if the superior orbital fissure is enlarged. It is also worth noting that a significant orbital apical anomaly, especially if the superior orbital fissure is enlarged, is associated with DVA of the brain and skull.5,21 On imaging, these lesions have an anterior component similar to that seen in LD lesions except that they usually have a posterior component that fills on DP-MDCTA and enlarges with Valsalva, demonstrating distensibility (Fig. 12). The presence of thrombosis is clinically associated with exacerbation, and contrast imaging shows a thrombus surrounded by enhancement (Figs. 13 and 14; Fig. 4 in accompanying article).37 Treatment Strategies. In terms of management, combined VD-LVMs can be observed unless there are functional or anatomical indications for treatment, in which case they can be excised and/or treated with sclerotherapy.68–70 Several surgical options may be considered. Clipping of an outflow vessel is possible (Fig. 14), particularly those with single vessel outflow. Alternatively, excision of the lymphatic component with mapping and gluing of the venous component is a more controlled option (Fig. 13). Packing or gluing of the apical venous

FIG. 14.  A, This young girl presented in March 2000 with a superomedial solid lesion that was associated with a deeper venous component that dilated on Valsalva maneuver (B). She was observed until she presented with a painful ecchymosis in January 2004 (C and D), which was due to an acute thrombosis (D, arrow) of the posterior distensible venous component (D, T1-weighted ­Gadolinium-enhanced MRI). The anterior component was a microcystic lymphatic component, and the posterior component was a distensible venous component. The anterior lesion was excised and the thrombosed posterior venous component clipped serially and then excised. E, The patient is shown 6 months postoperatively and has now 10 years of follow up without recurrence (F). Reprinted with permission from Rootman et al.21

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component can be performed following excision. Thrombogenic coils could be used for the venous component but may produce a painful exacerbation due to the acute thrombosis and may recanalize. Surgery can be facilitated by drainage and decompression of the anterior cystic components of the lesions to provide better visualization and more room. Also, more solid, no-flow LD components can be removed to facilitate access to the distensible component. Sclerotherapy can be used with caution to reduce these lesions as well.28,65,66,69,71–74 Lymphatic-Dominant LVMs. Lymphatic-dominant LVMs (also known as “lymphangiomas”) are composed mostly of lymphatic elements with histologically and hemodynamically less prominent venous elements that do not appear to change on dynamic assessment with Valsalva maneuver. They have neovascular tufts arising from the walls of the cysts, which may account for recurrent bouts of hemorrhage. Also, there are solid elements with sometimes dense lymphorrhages, collapsed lymphatic channels, stromal hemorrhages from friable vessels, scarring and inflammation, smooth muscle, and cysts (both serous and hemorrhagic (Fig. 11B).65 Clinically, they may present with recurrent swelling and inflammation and characteristically enlarge over years. When LD-LVMs are part of a complex facial distribution beyond the orbit, the patient usually has associated lesions in the

mouth and cheek and may have recurrent problems (swelling, intermittent hemorrhage, and inflammation). The mean age for presentation of the cases of LD-LVM tended to be older (average age, 13 years) than those with significant distensible venous components (VD-LVM), which had an earlier mean age of presentation of 6 years. The authors have noted that LD-LVM may even present as a lesion in adults, sometimes later in life (Fig. 11).60 CT shows irregular patchy contrast filling of the solid-appearing areas, often with clustered visible cysts that may have fluid–fluid levels. MRI is better at demonstrating the blood and serous/ proteinaceous fluid-filled cysts, both recent and old (Fig. 15A). When contrast is injected directly into these lesions, no outflow is demonstrated (Fig. 15B). MRI shows a mixture of solid and cystic components. The cysts may have variable content with menisci and late phase irregular contrast enhancement.75,76 Treatment Strategies. Management of LD-LVMs includes observation,77 sclerotherapy27,66 (although this group has found that sclerotherapy of macrocystic LMs has a higher efficacy than treating those primarily composed of microcysts), or surgery.21,64,66,78,79 Concerns have been raised about using traditional sclerosants (medical grade ethanol or sodium tetradecyl sulfate) in the deep orbit due to associated swelling and resultant increased mass effect (and consequent elevation of intraorbital pressure); however, their use has been described with good effect.28,80 Gentler agents (such as bleomycin and doxycycline) may have less postinjection inflammation and are options in management.80 Another management technique is to drain or excise the cysts to deal with acute expansion. Finally, it may be necessary to do gross total removal of the lesions, which can be aided by glue injection within the isolated network.21 A combination of sclerotherapy alone or followed by removal of the lesion is also an option.27

CONCLUSIONS The purpose of this review is to emphasize the role of investigation of hemodynamics in classification and treatment of vascular malformations. The authors have outlined their current thinking on the spectrum and management of orbital vascular malformations and have attempted to provide a conceptual model for understanding these complex challenges. Evolving and future treatment strategies for orbital lesions should be based on a better understanding of the pathophysiology and use of a common classification. Indeed, the standard of care and reporting should include dynamic assessment before, during, and after therapy.81–84 There are possibilities for new glue agents, sclerosants, or gels that could be left in the lesions, thereby curing them via minimally invasive image-guided methods.85–87 Also, as noted, serial injection of newer sclerosants may be useful in ablating and controlling progression of the lesions and may be combined with surgical interventions with and without gluing techniques. Other methods might include novel use of drugs,88,89 biologic targeting of the lesion’s endothelium, recanalization or relining the channels to stabilize them, reversal of the pathology perhaps with antiangiogenic90,91 and anti-inflammatory factors, or the use of endovascular techniques43 and physical agents.

REFERENCES FIG. 15.  A, T2-weighted MRI demonstrates a ­lymphatic-dominant lymphaticovenous malformation with solid and macrocystic components. B, Direct injection into another lymphatic-dominant lymphaticovenous malformation, demonstrating filling throughout the confined lesion without egress, which allowed for safe gluing and excision. B, Reprinted with permission from Rootman et al.21

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Vascular malformations of the orbit: classification and the role of imaging in diagnosis and treatment strategies*.

To describe the authors' experience with orbital vascular malformations using the International Society for the Study of Vascular Anomalies (ISSVA) cl...
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