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SPINAL AVMS

CLASSIFICATION AND SURGICAL MANAGEMENT OFSPINAL ARTERIOVENOUSLESIONS: ARTERIOVENOUSFISTULAE AND ARTERIOVENOUSMALFORMATIONS

Louis J. Kim, M.D.

Division of Neurological Surgery,Barrow Neurological Institute,

St. Josephs Hospitaland Medical Center,Phoenix, Arizona

Robert F. Spetzler, M.D.

Division of Neurological Surgery,Barrow Neurological Institute,St. Josephs Hospital

and Medical Center,Phoenix, Arizona

Reprint requests:

Robert F. Spetzler, M.D.,Neuroscience Publications,Barrow Neurological Institute,

350 West Thomas Road,Phoenix, AZ 85013.

Email: [email protected]

Received, January 25, 2006.

Accepted, June 14, 2006.

OBJECTIVE: Preexisting spinal arteriovenous malformation nomenclature can be con-fusing. The aim of this article is to present a modified classification system for spinalarteriovenous lesions and to discuss its implications for microsurgical strategies.

METHODS: Based on the literature review of prior classifications as well as on theexperience of the senior author (RFS), the authors delineate an anatomically andpathophysiologically based classification to facilitate the description and treatment ofthese uncommon entities.

RESULTS: Spinal arteriovenous lesions are composed of arteriovenous fistulae and

malformations. These lesions are classified as extradural, extradural-intradural, orintradural. Intradural lesions are characterized further as ventral or dorsal fistulae or asintramedullary lesions. Intramedullary lesions are characterized as compact or diffuse.A new category, conus medullaris arteriovenous malformations, is described as adistinct entity.

CONCLUSION: This updated classification system eliminates confusion related toolder nomenclature and is based on the anatomical and pathophysiological features ofthese lesions. When treating these lesions, the neurovascular team must collaborateclosely with their microsurgical and endovascular colleagues. Finally, treatmentshould be individualized, depending on lesional angioarchitecture and the patientsclinical status.

KEY WORDS:Classification, Nomenclature, Spinal arteriovenous fistula, Spinal arteriovenous malformation,

Surgical management

Neurosurgery 59:S3-195-S3-201, 2006 DOI: 10.1227/01.NEU.0000237335.82234.CE www.neurosurgery-online.com

Spinal arteriovenous lesions are a collection of disparateand diverse entities. Our understanding of their patho-physiology has evolved significantly over the past cen-

tury. As a byproduct of our gradual understanding of these

lesions, a cadre of nomenclature has developed over time.

Unfortunately, this terminology has served mostly to con-found rather than to facilitate accurate descriptions of spinal

arteriovenous malformations (AVMs). Recently, anatomicallybased classifications that offer accurate descriptions have beendeveloped.

In tandem with our understanding of the pathophysiology

of spinal AVMs, our technical ability to treat these lesions,both microsurgically and endovascularly, has improved tre-

mendously. This report describes the classification schemas of

spinal AVMs, pointing out the recent trend toward anatomicalnomenclature and the surgical strategies and techniques used

in the practice of contemporary neurosurgery.

CLASSIFICATION OF ARTERIOVENOUSFISTULAE AND AVMS

Spetzler et al. (44) proposed a modified classification systemfor spinal arteriovenous lesions based on specific anatomicaland pathophysiological factors. Descriptions are based on ex-tradural or intradural, ventral, dorsal, or intramedullary loca-

tions of the lesions and on the presence of single or multiplefeeding branches.

Extradural Arteriovenous Fistulae

Extradural arteriovenous fistulae (AVFs; Fig. 1), known asepidural fistulae in older nomenclature, represent an abnor-mal communication between an extradural arterial branchthat usually arises from a branch of a radicular artery and anepidural venous plexus. This entity results in significant en-gorgement of the venous system, leading to subsequent com-

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pressive mass effect on adjacent nerve roots and spinal cord.Venous hypertension and vascular steal also may contribute tomyelopathic symptoms.

Intradural Dorsal AVFs

Intradural dorsal AVFs (Fig. 2), which correlate with Type 1dural AVFs, are composed of a radicular feeding artery thatcommunicates abnormally with the venous system of the spi-

nal cord at the dural sleeve of the nerve root. Inherent to thepathophysiology is obstruction of spinal cord venous outflow,which ostensibly contributes to the formation of the fistula. Inturn, arterialization of the coronal venous plexus, venous hy-pertension, and myelopathy ensue.

Intradural Ventral AVF

Intradural ventral AVFs (Fig. 3) are ventral midline lesionslocated in the subarachnoid space. The fistulous site occurs be-tween the anterior spinal artery (ASA) and an enlarged venous

network. The lesions have been subclassified as Types A, B, andC (1). Type A intradural ventral AVFs are small and have a singlefeeder. The size of Type B lesions is intermediate. They have amajor feeder from the ASA and minor feeders at the level of the

FIGURE 1. A, axial illustration demonstrating an extradural AVF alonga perforating branch of the left vertebral artery (arrow). B , illustration ofthe posterior view demonstrating that engorgement of epidural veins can

produce symptomatic mass effect on adjacent nerve roots and spinal cord(courtesy ofBarrow Neurological Institute, Phoenix, Arizona).

FIGURE 2. A, axial illustration of an intradural dorsal AVF demon-strating an abnormal radicular feeding artery along the nerve root on theright. The glomerular network of tiny branches coalesces at the site of the

fistula along the dural root sleeve. B, illustration of the posterior viewdemonstrating the dilatation of the coronal venous plexus. In addition tovenous outflow obstruction (not shown), arterialization of these veins pro-duces venous hypertension. Focal disruption of the point of the fistula byendovascular or microsurgical methods will obliterate the lesion (courtesyofBarrow Neurological Institute, Phoenix, Arizona).

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fistula. Type C lesions are giant. They are multipediculated andhave massively dilated venous channels. Extraordinarily highflow through these lesions leads to the phenomenon of vascularsteal from the intrinsic spinal cord arterial supply and to thesequelae of ischemic symptoms.

Extradural-Intradural AVM

Extradural-intradural AVMs (Fig. 4) correspond with juve-nile or metameric AVMs. These formidable lesions are in-

vested along a discrete somite level. Typically, they involvebone, muscle, skin, spinal canal, spinal cord, and nerve roots.Complete involvement of an AVM along an entire somite levelhas been described as Cobbs syndrome.

Intramedullary AVMs

Intramedullary AVMs are analogous to intracranial AVMs,located entirely in the spinal cord parenchyma. These lesions

may have single or multiple feeding arteries from branches ofthe ASA and posterior spinal artery. They are classified fur-ther as compact or diffuse (Figs. 5 and 6), depending on theangioarchitecture of the nidus.

Conus Medullaris AVMs

Conus medullaris lesions (Fig. 7) occupy a separate category(44). Conus lesions typically exhibit multiple feeders from theASA and posterior spinal artery with direct arteriovenousshunts and large dilated veins. The pathophysiology underly-ing neurological decline includes venous hypertension, isch-emia, and mass effect from hugely dilated venous structures.Because the location and angioarchitecture of these lesions are

unique, both upper and lower motor neuron symptoms canoccur. Elimination of mass effect on descending nerve roots ofthe cauda equina can be associated with striking improve-ments.

DISCUSSION

Historical Perspective and Previous Classifications

In 1888, Gaupp (16) provided the earliest description of aspinal AVM. In 1910, Krause (25) reported the first surgically

FIGURE 3. A, axial illustration demonstrating an intradural ventral AVF, amidline lesion derived from a fistulous connection (arrow) between the anteriorspinal artery and coronal venous plexus. B, illustration of the anterior viewdemonstrating the fistula along the anteroinferior aspect of the spinal cord.Proximal and distal to this Type A lesion, the course of the anterior spinal arteryis normal (courtesy ofBarrow Neurological Institute, Phoenix, Arizona).

FIGURE 4. Axial illustration demonstrating an extradural-intraduralAVM. These treacherous lesions can encompass soft tissues, bone, spinal

canal, spinal cord, and spinal nerve roots along an entire spinal level.Considerable involvement of multiple structures makes these entitiesextremely difficult to treat. Although cures have been reported, the pri-mary goal of treatment is usually palliative (courtesy of Barrow Neuro-logical Institute, Phoenix, Arizona).

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treated spinal dural fistula, and in 1916, Elsberg (14) describedthe successful surgical treatment of a spinal epidural AVM. In1926, Foix and Alajouanine (15) reported the syndrome ofsubacute necrotic myelopathy associated with rapidly pro-gressive onset of paraplegia and subsequent death.

Subsequent investigators recognized that Foix-Alajouaninesyndrome was associated with spinal AVMs after acutethrombosis of the pathological vessels (28, 39). It is now un-

derstood that the syndrome can occur after acute exacerbationof underlying venous hypertension. If treated sufficientlyearly, the condition can be reversed in some cases. In 1943,Wyburn-Mason (49) reported 110 spinal AVMs, which heclassified histologically into arteriovenous angiomas andpurely venous angiomas. The latter category accounted formore than two-thirds of all cases. Consistent with Virchowsoriginal classification of vascular lesions, Wyburn-Mason per-petuated the older nomenclature by popularizing the terms

FIGURE 5. A, axial illustration demonstrating a compact intramedul-lary AVM. In this figure, an arterial feeder from the anterior spinal arteryis identified. Note the discrete, compact mass of the AVM. B, posteriorview demonstrating additional feeding branches from the posterior spinalartery and reemphasizing the compact nature of this type of spinal AVM.Portions of the AVM are evident along the surface of the spinal cord. Sur-

gical resection is the mainstay of treatment. Preoperative embolization isreserved for select cases only (courtesy of Barrow Neurological Institute,Phoenix, Arizona).

FIGURE 6. A, axial illustration demonstrating a diffuse intramedullaryAVM with areas of intervening neural tissue between the intraparenchy-mal loops of AVM. Portions of the AVM also course along the pial surfaceand subarachnoid space. B, illustration of the oblique posterior view dem-onstrating the loops of the AVM coursing in and out of the spinal cord.Normal neural tissue is evident between intraparenchymal portions of the

AVM. This view accentuates the diffuse character of these lesions (cour-tesy ofBarrow Neurological Institute, Phoenix, Arizona).

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for these lesions as angioma racemosum venosum and angiomaracemosum arteriovenosum (49).

As spinal angiographic techniques evolved (5, 1013), radio-graphic imaging of spinal AVMs afforded the opportunity todevelop anatomically based classifications. The most commonclassification scheme for spinal AVMs uses the Type 1 to 4

grading system (11, 13, 22, 29, 37). Type 1 lesions are duralAVFs in which a dural branch from a radicular artery forms anabnormal communication with the dural veins at the nerveroot sleeve. Arterialization of the perimedullary coronal ve-nous plexus results. Type 2 refers to glomus or intramedullarylesions. Type 3 lesions are juvenile or metameric AVMs asso-

ciated with both extradural and intradural extension of thespinal AVM. Type 4 spinal AVMs, as first described by Djind-jian et al. (12) and categorized as Type 4 by Heros et al. (22),refer to perimedullary fistulae. These ventrally located fistulaprimarily receive arterial contributions from the ASA.

Borden et al. (8) described a three-point classification forboth intracranial and spinal dural AVFs using the termduralarteriovenous fistulous malformation. Type 1 referred to extra-dural AVFs or epidural types, with direct drainage of thefeeding artery into Batsons venous plexus. Type 2 referred todural artery feeders draining into both epidural and intra-dural venous systems. Type 3 referred to what is known asintradural dorsal AVFs, or Type 1 AVMs, according to the

description of Di Chiro et al. (11).More recent spinal vascular lesion classifications are based

on descriptive anatomic considerations. Niimi and Berenstein(35) divided vascular lesions of the spine into spinal vascularlesions and spinal cord vascular lesions. They subdividedspinal vascular lesions into spinal dural fistulae and extra-dural fistulae. Spinal cord vascular lesions are referred to asspinal cord vascular malformations, of which there are two types:isolated, which includes AVMs and AVFs, and multiple,which includes metameric and nonmetameric forms.

Bao and Ling (6) classified spinal cord vascular lesions asintramedullary AVMs, intradural AVFs, dural AVFs, paraver-tebral AVMs, and Cobbs syndrome. Intramedullary lesions

include glomus and juvenile forms. Intradural AVFs are sub-divided into Types 1 to 3, as the size of the lesion and degreeof AVF flow increase.

Rosenblum et al. (42) differentiated spinal AVFs fromAVMs based on their experience with 81 treated patients.Intradural AVMs were divided into intramedullary and directAVFs. Intramedullary lesions included glomus and juvenileAVMs. Direct AVFs occupied either an intramedullary orextramedullary location. Intramedullary lesions were sup-plied by medullary arteries, and the arteriovenous shunt waslocated partially in the spinal cord or pia mater. Dural AVFswere supplied by a radicular branch along the dural nerveroot sleeve, which drained via an AVF into the coronal venous

plexus.Our classification system represents an evolution that incor-

porates our enhanced understanding of these entities in recentdecades (7, 27). This classification system offers several advan-tages. First, it includes all spinal AVFs and AVMs, includingthe recently proposed conus medullaris category (41, 44). Sec-ond, the system is based on the anatomic location of eachlesion with its corresponding pathophysiological mechanism.Finally, it eliminates potential confusion inherent in the oldernomenclature.

FIGURE 7. A, axial illustration demonstrating a conus medullaris AVMand the feeding arteries and draining veins from both the anterior and

posterior aspects of the spinal cord. Note the proximity of the AVM tobranches of the cauda equina. B, illustration of the posterior view recapitu-lating the complexity of the angioarchitecture of these lesions. Anteriorand posterior spinal arteries, radicular arteries, and anterior and posteri-orly draining veins are involved simultaneously. Portions of the AVM canconsist of direct AV shunts as well as regions of true AVM nidus. Dur-

ing endovascular treatment, surgical treatment, or both, it is crucial toidentify the en passage branches of the anterior and posterior spinal arter-ies (courtesy ofBarrow Neurological Institute, Phoenix, Arizona).




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Treatment Strategies

Three pathophysiologic mechanisms underlying spinalAVMs can cause neurological injury: hemorrhage, mass effect,or vascular steal. Venous hypertension tends to be associatedwith either intradural spinal AVFs or conus medullaris-type

spinal AVMs. Clinical manifestations can include pain, acuteor progressive myelopathy, and radiculopathy. Magnetic res-onance imaging and a thorough catheter-based angiogramprovide the most important diagnostic information.

In contemporary neurosurgical settings, these lesionsshould be approached in a team-oriented fashion. Optimalpatient care depends on direct collaboration between openvascular and endovascular neurosurgeons. The role of eachhalf of this neurovascular team depends on the lesion, andtreatment must be individualized to the specifics of each sit-uation. The following surgical strategies and technical consid-eration serve only as a guide.

At our institution, monitoring somatosensory and motorevoked potentials has become a routine part of spinal AVMsurgery. Intraoperative angiography should be used in se-lected cases when residual AVM may remain. When intraop-erative angiography is unwarranted or indeterminate, imme-diate postoperative, as well as long-term, follow-up catheter-based angiography is the mainstay of our treatment paradigm.

Surgical Management

Extradural AVFs are treated primarily by endovasculartechniques (3, 18, 21, 32, 35, 43). In our experience, the purelyextradural fistula is an extremely uncommon lesion. The roleof surgery in treating these lesions is limited to patients re-quiring reduction of local compression.

In 1977, Kendall and Logue (24) accurately redefined thepathophysiology of intradural dorsal AVFs. They recognizedthat the fistulous point occurred at the level of the dural rootsleeve rather than along the dilated coronal venous plexus,which can be striking in such patients. Earlier, it was common toperform vein stripping procedures with no benefit or even wors-ening of symptoms (26) and with no effect on obliteration of thefistula itself. It is worth reiterating that successful surgical man-agement of these lesions requires a careful and thoroughcatheter-based spinal angiogram to identify the arterial feeder(s)and artery of Adamkiewicz. Although angiographic visualiza-tion is paramount, angiographically occult lesions in patientsunder high clinical suspicion for intradural dorsal fistulae havebeen associated with successful surgical exploration and fistuladisruption (36). These rare instances stress the importance ofrecognizing the clinical manifestations of these fistulae.

As soon as the appropriate spinal level has been identified, thesurgical strategy involves its posterior exposure. We favor aposterior approach and laminoplasty. High-powered magnifica-tion and illumination with the operating microscope are used toperform intradural dissection along the appropriate nerve root.Typically, an arterialized vein is identified along the nerve rootand can be dissected sharply to its exit point at the margin of thedural root sleeve. Nonstick bipolar cauterization and microscis-

sors are used to interrupt the fistula. The advantage of surgicaldisruption is the relative ease of exposure and direct visualiza-tion of the vascular anatomy (2, 33, 36, 38, 42, 46).

Small intradural ventral AVFs (Subtypes A and B) are man-aged surgically (1, 17, 20, 40). These lesions may require ananterior or anterolateral approach for adequate exposure; how-

ever, posterolateral approaches are feasible for ventrolateral le-sions (23, 30). Therefore, a thorough understanding of complexspinal approaches is essential for both the operative approachand spinal stabilization. Key to surgical success is preservation ofthe ASA branches during obliteration of the fistula. Giant (Sub-type C) lesions, however, are best treated with endovascularembolization techniques because of their complex angioarchitec-ture and multipedicled feeders (1, 19, 22, 31, 34, 40).

Extradural-intradural AVMs are formidable lesions involv-ing neural structures, bone, and soft tissue along the affectedspinal level. They are treated primarily with endovascularembolization; surgery is reserved for decompression of masseffect along the nerve roots and spinal cord (22, 29, 30, 35, 38,

45). Although treatment cures have been reported (30, 45, 47),the realistic goal in most cases is reduction of mass effect,venous hypertension, and vascular steal to ameliorate thepatients neurological deficits.

Intradural-intramedullary AVMs have been treated success-fully with embolization procedures (4). However, the main-stay of treatment remains surgical extirpation (9, 44). Werecommend preoperative embolization in selected cases, par-ticularly for patients with complex, multipedicled lesions.Typically, a posterior or posterolateral approach is suitable,but an anterior approach may be warranted in selected cases(9, 30, 48). For diffuse lesions (Fig. 6) situated superficially onthe spinal cord, it is prudent to avoid chasing vascular loops of

AVM that may invaginate into the spinal cord parenchyma.Because the pathophysiology of this lesion defines it as asuperficial entity, it is best to truncate vessels embedded in theparenchyma at the pial surface. This strategy minimizestrauma to the tissue that could lead to inadvertent neurolog-ical injury yet still permits complete obliteration of the lesion.We have achieved gross total resection of 92% of the intramed-ullary AVMs that we have treated (44).

Conus medullaris AVMs are treated with a combined en-dovascular and microsurgical approach. Careful identificationof ASA and posterior spinal artery branches separate from thelesion is crucial. Because the venous structures associated withconus AVMs are so hugely dilated, surgical decompression ofadjacent spinal cord and nerve roots can relieve neurologicalsymptoms significantly. Conus AVMs are usually easily ac-cessible from a posterior approach. Our continuing experiencewith these entities has demonstrated that aggressive com-bined treatment can result in good outcomes (44).

CONCLUSION

Our ability to identify and treat spinal AVMs has advancedtremendously in the past several decades. This article de-scribes a modified classification system of spinal arterio-

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venous lesions based on this current anatomic and pathophys-iological understanding. Further advances in the treatment ofspinal AVMs mandate an integrated approach with microvas-cular and endovascular neurosurgeons.

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