Spinal arteriovenous malformations: new classification and ...ficulties are caused by the lack of a...

PINAL vascular malformations represent a rare andinsufficiently studied pathological entity character-ized by considerable variation.2,5,7,12,14,20,22 These le-

sions have been insufficiently studied because of the com-plexity of their diagnosis, which restricts the developmentof surgical treatments that are differentiated according tothe type of malformation.9,13 Great difficulties are causedby lack of a clear structural–hemodynamic classificationof spinal AVM. At present, the classification created be-tween 1991 and 1998 by the combined efforts of differentauthors is the one most widely used. According to thisclassification, the following four categories are distin-guishable: Type I, dural AVFs; Type II, intramedullaryglomus AVMs; Type III, juvenile or combined AVMs; andType IV, intradural perimedullary AVFs.2,3 Vascular tu-

mors are also identified: hemangiomas, hemangioblasto-mas, angiosarcomas, hemangiopericytomas, angiofibro-mas, angiolipomas, and hemangioendotheliomas, as arecavernous malformations.19

In 2002 Spetzler, et al.,19 offered a new classification ofspinal vascular pathological entities. Nevertheless, this clas-sification does not cover the whole spectrum of spinal mal-formation types. Therefore, we consider a detailed system-atization of spinal vascular malformations to be necessary;such a scheme can facilitate the development of tactics forsurgical interventions that are differentiated with regard tothe localization, angiostructural type, and hemodynamicpeculiarities of malformations and will allow optimizationof the results of treatment.

Clinical Material and Methods

In this study we analyzed the diagnostic data and resultsof treatment in 91 patients with AVMs and AVFs whowere treated at the Institute of Neurosurgery between

Neurosurg. Focus / Volume 20 / May, 2006

Neurosurg Focus 20 (5):E7, 2006

Spinal arteriovenous malformations: new classification andsurgical treatment

YURI P. ZOZULYA, M.D., PH.D., EUGENE I. SLIN’KO, M.D., PH.D., AND IYAD I. AL-QASHQISH, M.D.

Institute of Neurosurgery, Kiev, Ukraine

Object. Spinal vascular malformations represent rare and insufficiently studied pathological entities characterizedby considerable variation. Insufficient study of this disease is connected with the complexity of its diagnosis, whichrestricts the development of surgical treatments that are differentiated according to the type of malformation. Great dif-ficulties are caused by the lack of a clear structural–hemodynamic classification of spinal arteriovenous malformations(AVMs). At present the classification created between 1991 and 1998 by the combined efforts of different authors isthe most widely used one. According to this classification, four categories are distinguishable: Type I, dural arteriove-nous fistulas (AVFs); Type II, intramedullary glomus AVMs; Type III, juvenile or combined AVMs; and Type IV,intradural perimedullary AVFs. Vascular tumors are also classified, as follows: hemangiomas, hemangioblastomas,angiosarcomas, hemangiopericytomas, angiofibromas, angiolipomas, and hemangioendotheliomas, as well as cav-ernous malformations.

Methods. In this study the authors analyze the diagnostic data and results of treatment in 91 patients with AVMsand AVFs who were treated at the Institute of Neurosurgery between 1995 and 2005. The patients’ ages ranged from9 to 83 years; the mean age was 42.9 years. For spinal vascular malformations we devised a classification that tookinto account the aforementioned features of AVMs: the anatomical characteristics of a malformation and its angiostruc-tural and hemodynamic features. In all patients the neuroimaging modalities used in the investigation of their lesionsincluded magnetic resonance (MR) imaging and selective spinal angiography. Three-dimensional computerized tomo-graphy angiography studies were obtained in 14 patients, and MR angiography was used in 17.

Conclusions. For successful surgical treatment of spinal AVMs it is necessary to obtain data about their localiza-tion, vascular structure, and hemodynamics that are as complete as possible. This information will promote the use ofoptimum surgical procedures and the latest methods of microsurgical and endovascular interventions, with treatmentsdifferentiated according to the type of malformation. One should try to use the least invasive endovascular approachin these cases,where possible, to occlude the AVM or reduce the intensity of blood flow by means of embolization. Toperform an AVM resection or occlusion, one should use a direct approach to the malformation, blocking only the ves-sels supplying blood to the malformation and preserving the vessels feeding the spinal cord.

KEY WORDS • spinal arteriovenous malformation • structural–hemodynamic classification •surgical treatment

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Abbreviations used in this paper: AVF = arteriovenous fistula;AVM = arteriovenous malformation; MR = magnetic resonance;VA = vertebral artery; VB = vertebral body.

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1995 and 2005. The patients’ ages ranged from 9 to 83years; the mean age was 42.9 years. For spinal vascularmalformations we devised a classification that took intoaccount the aforementioned features of malformations:anatomical characteristics of a lesion and its angiostruc-tural and hemodynamic features (Table 1). Based on theiranatomical features, AVMs are divided into intramedulla-ry, perimedullary, dural, epidural, intravertebral, and com-bined (covering some adjacent areas). The feeding anddraining vessels were designated because many malfor-mations had essential differences depending on the supplyvessels. Aneurysms of spinal vessels were observed in ourstudies only in combination with AVMs. Hemodynamicdifferences and differences in vascular structure in manycases required different surgical tactics. We did not in-clude spinal vascular tumors and cavernous malforma-tions in this study because they represent separate patho-logical entities.

In all patients the evaluations included MR imaging andselective spinal angiography. Three-dimensional comput-erized tomography angiography studies were obtained in14 patients and MR angiography in 17.

Surgical intervention was performed in all 91 patients:in 13 of them endovascular interventions were applied, in70 we performed microsurgery, and in eight we performedcombined operations with application of endovascular andmicrosurgical techniques. During open operations, dorsaland dorsolateral approaches were chiefly used. Ventraland ventrolateral approaches were used in eight patients,and in 11 patients operative interventions were completedby stabilization of the spine.

Statistical analysis (digital neurological scales, t-criteri-on, and comparison of these data before and after the oper-ation) was conducted using the program Microsoft Excel2002 and its statistics supplement Analysis ToolPak. Cor-relative, cluster, and linear regression analyses were per-formed using the STATISTICA program (version 6;StatSoft, Inc., Tulsa, OK).

Results

Types of Malformations

Intramedullary AVMs. For intramedullary AVMs of allkinds, clustering zones of low-intensity MR signals in thespinal cord were typical. The spinal cord seemed expand-ed in the region of the malformation; sometimes expand-ed perimedullary draining veins were discovered aroundthe cord on MR images. Changes of the spinal cord densi-ty were observed around the vascular nidus. The size anddensity of arrangement of the malformation’s vessels var-ied essentially. The vessels were densely packed in glo-mus AVMs and scattered in the spinal cord in diffuseAVMs in which the spinal cord matter was observedamong the vessels. The selective spinal angiography stud-ies revealed a vascular conglomerate consisting of vesselsthat either adjoined each other tightly (glomus type) orwere scattered in the spinal cord matter (diffuse type).Direct AVM feeding vessels passed from the ventral ordorsal spinal arteries, and sometimes from the radiculopi-al arteries. The AVM was drained by the perimedullaryveins. According to the MR imaging and surgical find-ings, intramedullary AVMs were limited by spinal cord or

the conglomeration of vessels spread on the surface of thespinal cord (Figs. 1–6).

Intradural or Perimedullary AVMs. These lesions werevisualized on MR imaging as conglomerations of vesselsin the form of low-intensity zones around the spinal cordon MR images. These vessels could be localized on theventral as well as on the dorsal or lateral spinal cord sur-face. The spinal cord was not expanded; in most cases itscompression and displacement by the malformation wasobserved. Spinal cord edema was rare with this type ofmalformation. The selective spinal angiography studiesdemonstrated feeding vessels from the ventral or dorsalradiculomedullary arteries. Comparing the MR imagingand selective spinal angiography data, we often foundthrombosis in AVM vessels. These vessels drained intothe ventral or dorsal perimedullary veins (Figs. 7 and 8).

Intradural or Perimedullary AVFs. In perimedullaryAVFs, MR imaging demonstrated a serpentine pattern ofvessels around the spinal cord, although in contrast toAVMs, there were no vascular conglomerates, signs ofcompression, or displacement of the spinal cord. In thepatients with AVF in whom insignificant blood shuntingoccurred, the perimedullary veins on the spinal cord sur-face were hardly noticeable. As distinct from the perime-dullary AVMs, spinal cord edema was marked in theAVFs. The typical finding on selective spinal angiographywas an AVF in the form of a direct passage of the feedingvessel (the ventral or dorsal spinal artery) into the drain-ing ventral or dorsal perimedullary veins.

As a rule, with ventral feeding vessels, an AVF drainedinto ventral perimedullary veins and vice versa, whereaswith dorsal feeding vessels an AVF drained into the dorsalperimedullary veins. The draining veins were twisted andcould be traced for a long distance along the spinal cord.In AVFs, the feeding vessels more often were the ventralor the dorsal spinal arteries, whereas in AVMs they werethe ventral or dorsal radiculomedullary arteries. In vascu-lar malformations arising in the conus medullaris, thefeeding vessels coursed with the cauda equina roots.Based on the amount of blood shunting nd the size of thelesion, perimedullary AVFs and AVMs were divided intolesions with the following characteristics: A) insignificantblood shunting; B) moderate blood shunting; or C) con-siderable blood shunting (Figs. 9–13).

Dural AVMs and AVFs With Retrograde Drainage IntoPerimedullary Veins. In dural AVMs and AVFs with retro-grade drainage into perimedullary veins, expansion ofthese veins was found on MR imaging studies. DuralAVMs or AVFs of the thoracic region were more oftendrained into the dorsal perimedullary veins. Rare duralAVFs of the cervical spine could be drained into the ven-tral perimedullary veins. In patients with an insignificantamount of blood shunting, the perimedullary vein expan-sion looked like serpiginous flow voids on the dorsal sur-face of the spinal cord, most often in the middle and lowerthoracic spine. In case of moderate blood shunting, ex-panded veins were found on the T1- and T2-weightedsequences in the form of a serpentine vascular pattern inthe subarachnoid space. In all cases, vast spinal cordedema and thickening were typical. Angiographic studiesrevealed expanded radiculomeningeal arteries, whichdirectly (in AVFs) or through a vascular conglomerate in

Y. P. Zozulya, E. I. Slin’ko, and I. I. Al-Qashqish

2 Neurosurg. Focus / Volume 20 / May, 2006


the region of the intervertebral neural foramen (in AVMs),shunted into the expanded perimedullary veins. Mostoften, a malformation had only one tributary and wascharacterized by slow blood flow; several tributaries wererarely found. The blood flow in spinal cord arteries wasalso slower. It was especially noticeable when contrastmaterial was added in the artery of Adamkiewicz. Thisoccurred because spinal as well as cerebral dural malfor-mations are found against a background of venous hyper-tension, which is considered the initial cause of dural mal-formations (Figs. 14 and 15).

If a dural AVM or AVF had antegrade epiduraldrainage, on MR images there were prominent venouspouches in the epidural space. These pouches had a roundor ellipsoid form and stretched along the one to three ver-tebrae. The characteristic features of such lesions wereinsult-like ischemic changes of the spinal cord thatappeared as an area of low MR signal intensity in the T1-weighted and high intensity in the T2-weighted sequences,and as an edema around the cord. Enlarged perimedullaryvessels are not typical. Expanded radiculomeningeal arter-

ies were discovered on angiographic studies; these arter-ies shunted directly (in case of AVF) or through a vascu-lar conglomerate into the expanded epidural veins, whichshunted through the veins passing through the interverte-bral foramina.

Epidural AVMs and AVFs. These lesions were character-ized by low-intensity-signal zones located epidurally onMR imaging, and had caused a compression of the duramater. Selective spinal angiography obtained with contrastagents demonstrated the feeding vessels spreading outdirectly from the spinal branch or from the postcentral,prelaminar branches. The vascular conglomerate of theAVM or AVF was not large; it consisted of small vessels.In contrast to dural AVFs and AVMs, these lesions werelocated, not in the region of the intervertebral foramen anddural sleeve of the nerve root, but in the epidural space.The lesions were drained rostrally or caudally through theepidural veins. Sometimes the drainage through the inter-vertebral veins at the level of the malformation passed toparavertebral veins (Fig. 16).


Spinal AVMs: new classification and surgical treatment

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TABLE 1Classification of spinal AVMs*

Localization Vascular Structure Hemo-dynamic

Axial Lengthwise Feeding Vessels Structural Features Drainage Features

I. intramedullary 1. cervical 1. ant spinal artery 1. glomus or compact AVM 1. perimedullary veins A. low flow2. thoracic 2. pst spinal artery 2. diffuse AVM B. mod flow3. conus medullaris 3. radiculopial artery C. high flow

4. combinedII. intradural or 1. cervical 1. ant spinal artery 1. glomus AVM 1. ant perimedullary A. low flow

perimedullary 2. thoracic 2. ant radiculomedul- 2. AVF veins B. mod flow3. conus medullaris lary artery 2. pst perimedullary C. high flow

3. pst spinal artery veins4. pst radiculomedul-

lary artery5. combined

III. dural 1. cervical 1. radiculomeningeal 1. microglomus AVM 1. retrograde into ant A. low flow2. thoracic artery 2. AVF perimedullary veins3. lumbar 2. retrograde into post

perimedullary veins3. antegrade into epidural

veinsIV. epidural 1. cervical 1. VAs 1. glomus AVM 1. epidural veins A. low flow

2. thoracic 2. spinal branch of 2. AVF 2. paravertebral veins B. mod flow3. lumbar segmental arteries C. high flow

3. postcentral branches 4. prelaminar branches 5. combined

V. intravertebral 1. cervical 1. ventrolateral branches 1. glomus AVM limited 1. epidural veins A. low flow2. thoracic of segmental arteries by vertebra 2. paravertebral veins B. mod flow3. lumbar 2. postcentral branches 2. glomus AVM w/ para- 3. combined C. high flow

3. prelaminar branches vertebral spreading4. combined

4.1 one side 4.2 both sides

VI. combined 1. cervical 1. mainly from spinal 1. mainly intradural 1. mainly perimedul- A. low flow2. thoracic branches glomus AVM lary veins B. mod flow3. lumbar 2. mainly from radicu- 2. mainly extradural 2. mainly epidural C. high flow

lomedullary arteries glomus AVM veins3. mainly paravertebral

veins4. combined

* Ant = anterior; mod = moderate; pst = posterior.


Intravertebral AVMs. According to the MR imagingdata, intravertebral AVMs were discovered in the form oflarge vessels with intense blood flow, which were situatedmore often inside the vertebrae or with paravertebralspreading from these structures. Expanded epidural orparavertebral veins draining these AVMs were visible onMR images. Selective spinal angiography was used to

identify AVM feeding vessels from the ventrolateralbranches of segmental arteries (postcentral and prelaminarbranches). The AVMs were drained through the epiduralor the paravertebral veins into the ascending lumbar veins,the inferior vena cava, and the azygos and hemiazygosveins (Fig. 17).



FIG. 1. Sagittal (A) and axial frontal (B) MR images demon-strating an intramedullary diffuse AVM at the C-5 level. The openarrows designate the intramedullary AVM nidus.

FIG. 2. Vertebral angiograms demonstrating an intramedullary diffuse AVM at the C-5 level. A and B: Preoperativeimages, frontal and lateral projections. C and D: Angiograms obtained in frontal and lateral projections after the AVMresection. 1 = feeding vessels; 2 = the AVM nidus.

FIG. 3. Intraoperative photographs showing an intramedullarydiffuse AVM at the C-5 level. A: A conglomeration of per-imedullary draining veins is seen. B: The veins have been coag-ulated, and myelotomy has been performed in the root entry zonein front of the posterior roots. The roots have been moved asidedorsally with a rubber retractor. The vessels of the nidus within thespinal cord have been coagulated and cut off.


Combined Malformations. Combined lesions were situ-ated in several adjacent anatomical structures. If combin-ed glomus AVMs were located mainly intradurally, theyreceived tributaries chiefly from the radiculomedullaryarteries and had perimedullary venous drainage. In case ofprimary extradural localization, the combined glomera ofthe AVMs received tributaries from the spinal branchesand were drained mainly by the epidural and paravertebralveins. However, these AVMs often had equally intraduraland extradural locations (Figs. 18 and 19).

Surgical Interventions

Based on the MR imaging and angiography data wecollected, the operative intervention was planned. Thechoice of surgical tactic depended on the localization, vas-cular structure, the ways of inflow and outflow, and hemo-dynamic peculiarities of the lesions. As a rule, in AVMs

the feeding and draining vessels needed to be occludedand a resection of the malformation was necessary. InAVFs it was enough to occlude only the feeding vessels.

The indications for occluding only the feeding vesselswere as follows: an intramedullary diffuse AVM (becausethe diffuse character of the AVM could lead to an exten-sive surgical injury to the spinal cord during an attempt toperform nidus resection); a perimedullary AVF; an intra-vertebral AVM; a combined AVM; or a dural AVF orAVM. In some cases of dural malformation it was optimalto occlude the draining vessels only.

The occlusion of the feeding and draining vessels andmalformation resection were necessary in the followingcases: intramedullary glomus AVM; perimedullary AVM;epidural AVM; and combined AVM.

The type of surgical intervention was determined inaccordance with the chosen surgical tactics. Endovascularembolization was performed when there were indications



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FIG. 4. Neuroimages demonstrating an intramedullary glomus AVM arising mainly in the right half of the spine, withexophytic spreading dorsolaterally at the T9–12 level. A–D: Preoperative MR images demonstrating the lesion’s sta-tus. E–H: Postoperative MR images revealing no signs of blood flow.


for occlusion of only the feeding vessels. Embolization ofthe main vessels is possible only if they do not take part inthe spinal cord blood supply, but provide blood to the vas-cular malformation only. In cases in which the main seg-mental vessel supplies the vascular malformation buttakes part in supplying the spinal cord blood, only super-selective obliteration of the malformation’s direct tribu-taries is possible.

Open microsurgery is necessary for resection of anAVM nidus. Open surgical interventions are advisablealso when it is necessary to occlude only the feeding ves-sels, but one has failed to embolize them endovascularly,or if embolization of the main tributaries threatens toocclude the arteries feeding the spinal cord. Microsurgicalinterventions are also advisable if a vascular formation hasthe kind of structure in which there is a collateral bloodflow and embolization of the main tributaries will notresult in complete occlusion of the blood flow; or if selec-tive spinal angiography does not identify all of the tribu-taries or there are suspiciously few of them, and their

diameter is too small in comparison with the presumableone, according to the MR imaging data.

Combining surgical intervention with endovascularembolization that is performed before the microsurgicalprocedure is advisable if it is necessary to resect an AVMthat has a high flow and numerous large feeding vesselsrunning into it, or if after the endovascular embolization amass effect due to AVM blood flow remains.

For endovascular embolization, two variations of theconventional technique were applied: 1) superselectiveobliteration of the feeding vessels; and 2) obliteration ofthe main tributary, usually the segmental artery. The firstmethod was applied in cases in which either the main seg-mental vessel supplied blood simultaneously to the mal-formation and the radiculomedullary arteries or the mal-formation’s blood was supplied directly from the anterioror dorsal spinal arteries. If these arteries ended in theAVM or the AVF, it was possible to apply selective embol-ization. If these arteries extended branches to the AVM orthe AVF and continued farther, feeding the spinal cord, we



FIG. 5. Selective spinal angiography studies of an intramedullary glomus AVM demonstrating four tributaries. Aand B: Arterial- and venous-phase angiograms obtained in the anterior radiculomedullary artery, which arises from thespinal T-9 branch on the left. C–E: Angiograms demonstrating the radiculopial T-10 artery branching from the rightsegmental artery. F: The anterior radiculomedullary T-10 artery branching from the left segmental artery is demon-strated. G–I: Angiograms demonstrating the dorsal radiculomedullary T-11 artery branching from the right segmentalartery. An intramedullary conglomeration of vessels is seen at the T-9 level. The two draining veins run rostrally and cau-dally.


avoided embolization. The second method of emboliza-tion, a nonselective technique of obliteration of the seg-mental main tributary, was applied if this artery did notfeed the spinal cord (Table 2).

If there were several tributaries, we performed anendovascular obliteration of all arteries during one opera-tion. Later it became obvious that such a method led toneurological deterioration. That is why we now apply themethod of staged obliteration of tributaries (no more thanone per operation) with a few days between each stage.

Surgical approaches in cases of intramedullary AVMdepended on the type of feeding vessels and the primarylocation of the nidus. In lesions with feeding vessels fromthe anterior spinal artery and the malformation’s locationin the ventral regions of the spinal cord or its exophyticspreading, we use ventral approaches; a ventral paratra-cheal cervical, transthoracic, or costotransversectomyapproach in the thoracic spine. These approaches providea direct route to the feeding vessels and the nidus, and theyrequire no spinal cord traction.

In cases of tributaries from the dorsal spinal arterieswhen the AVM is situated in the dorsal regions of thespinal cord or when there is dorsal exophytic spreading,

posterior approaches are chosen. In microsurgical resec-tions of intramedullary glomus AVMs, two variants ofnidus resection were applied: 1) first the tributaries anddraining vessels near the nidus were isolated and coagu-lated, then the nidus was dissected from the spinal cord,and resection of the AVM was performed; or 2) the ves-sels of the AVM nidus were “untangled,” the feeding andthe draining vessels were cut off in the nidus itself duringits separation, and resection of the nidus was performed atthe final stage. The last technique is more adequate if theAVM has feeding vessels from the anterior and posteriorspinal arteries. First we cut off the tributaries from theposterior spinal arteries, and then we perform a myeloto-my, identify, and cut off the individual vessels inside thenidus. Gradually, along the midline, we pass through thespinal cord ventrally, and in the ventral regions of thespinal cord we identify and cut off the feeding vesselsfrom the anterior spinal artery. As a rule, these are expand-ed central branches of anterior spinal artery. Inintramedullary diffuse AVMs, we cut off the feeding ves-sels near the nidus, then we performed a myelotomy, par-tially isolated the vessels in the nidus, coagulated andintersected them, but left them in situ. This provided theAVM with total occlusion, but taking into account diffusepenetration of the spinal cord by vessels and the presenceof spinal tissue among the vessels, the method of leavingvessels in situ allowed us to reduce the spinal cord injuryduring operation. In cases of intramedullary glomus AVMof the conus medullaris, because of the possible pelvicdisturbances, we only performed occlusion of AVM feed-ing vessels, leaving the malformation in situ (Figs. 1–6).

If perimedullary AVMs were present, the microsurgicaltechnique included occlusion of the feeding vessels rightat the nidus as the first step, then the draining per-imedullary veins were cut off, and total resection of theAVM was performed. During this procedure, we tried topreserve the pial vascular plexus of the spinal cord. Theperimedullary AVM in our studies had tributaries from theanterior and dorsal radiculomedullary arteries. We chosethe dorsal approach because these arteries stretched alongwith the roots, which allowed us to isolate them and cutthem off easily after facetectomy. In lesions with ventraldrainage, ventral perimedullary draining veins were cutoff via the dorsolateral approach (Figs. 7 and 8).

In cases of perimedullary AVF, the feeding vessels werecut off just before their inflow into the draining veins.When the blood flow was massive, the endovascular tech-nique or combined interventions were used; the microsur-gical technique was used when the blood flow wasinsignificant or moderate. When the fistula was fed fromthe posterior spinal arteries, the dorsolateral approach waschosen, and the feeding vessels were cut off at the point oftheir transition into the perimedullary veins, based on theangiograms. When the fistula was fed from the anteriorspinal artery, the ventrolateral approach was chosen and,after the feeding vessels were cut off, a spine fusion wasperformed (Figs. 9–12).

With dural AVMs and AVFs, two variants of surgicaltechnique were applied: 1) occluding the fistula or themalformation in the dural leaf of the spinal nerve root orcutting off the feeding vessels immediately outside theroot; or 2) occluding the radicular vein, which provides



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FIG. 6. Intraoperative photographs of an intramedullary glomusAVM at the T9–12 level. A: Vascular conglomerate with exo-phytic spreading. B: Intraoperative appearance after theintramedullary conglomeration has been removed. C:Photograph of the resected intramedullary AVM.


retrograde blood shunting from the AVF or the AVM intothe perimedullary veins. The first method was more com-plicated; it required a facetectomy as well as wide isola-tion of the root and its dural leaf opening. This methodsometimes resulted in irritation of the root and radicularpain postoperatively. In the second variant, the surgicaltechnique was similar for dural AVM and AVF becausewe did not directly expose the fistula or the malformation.This variant technique essentially reduced the possibilityof recurrences. With the use of the first method, the fistu-la or the malformation could recur due to the developmentof collateral vessels of the radicular arteries, which shunt-ed into the radicular veins. Because of the lack of a shunt-ing radicular vein, after application of the second methodthere was no possibility of recurrence. In all cases we usedthe dorsal approach. It is easier to cut off the dorsal radic-ular vein because it passes with the nerve roots toward the

dorsal spine surface. The vein is coagulated and sectioned.The ventral radicular vein passes with the nerve roots to-ward the ventral spine surface. To uncover this vein, par-tial facetectomy and exposure of the ventral roots is nec-essary. We apply the first variant of surgical techniquesonly for dural AVMs and AVFs that have antegrade drain-age into the epidural veins. In such cases, along with cut-ting off the tributaries, we coagulated the epidural veinsinto which the fistula drained (Figs. 14 and 15).

To occlude epidural AVMs and AVFs, only microsurgi-cal techniques, dorsolateral approaches, and total or par-tial facetectomy were used. In the region of the interverte-bral foramen, we coagulated and sectioned the directtributaries: postcentral, prelaminar spinal branches.Sometimes we coagulated and sectioned the spinal branchof the segmental artery laterally at the point of its entry in-to the intervertebral foramen. We completely coagulated



FIG. 7. Neuroimaging studies of a perimedullary AVM at the T10–L2 level. The vascular conglomerate is locatedaround the spinal cord. A–D: Preoperative T2-weighted sequences, sagittal sections. E: Preoperative MR image,frontal section. F: Axial section, T1-weighted sequence. G: Postoperative MR images acquired in T1- and T2-weight-ed sequences, demonstrating total removal of the malformation. 1 = vessels of the conglomerate; 2 = thrombosedaneurysm; 3 = anterior vein draining in the caudal direction; 4 = feeding vessel at the L-1 level coursing from the left; 5 = dorsal vein draining in the rostral direction; 6 = spinal cord.


the intervertebral veins, and in addition we partially coag-ulated the epidural veins. Then we coagulated and sec-tioned the point of the fistula or removed the AVM. If theepidural draining veins compressed the dural sac, theywere coagulated. When treating an epidural AVF feedingfrom the VA, we prefer the endovascular technique (Fig.16).

For intravertebral malformations, we combine endovas-cular obliteration of feeding vessels and direct surgicalintervention. To remove intravertebral vascular forma-tions situated in the dorsal structures of the vertebrae, thestandard dorsal approach was used. If the VB was affect-ed but there was no body expansion and dura mater com-pression, for obliteration of vascular formations affectingthe VBs, a percutaneous or intraoperative vertebroplastywas used. The VB was filled with bone cement in a vol-ume up to 8 ml. For intervertebral malformations affectingonly the VBs with their expansion, we performed ventralapproaches with ventrolateral and spinal branches of thesegmental arteries or the segmental branches themselvesto occlude the vessels and resect the affected VB.

With combined AVMs, we applied either endovasculartechnology only, when there was primary extradural local-ization, or we used a combination of endovascular andmicrosurgical methods when there was mainly intradurallocation and spinal cord compression (Figs. 18 and 19,and Table 2).

In all 91 patients who underwent operation, total cutoffof the vascular malformation from the blood flow was asuccess. As mentioned earlier, in cases of AVF the inter-vention entailed cutoff of the fistula, in cases of AVM weperformed total nidus resection, and in cases of diffuseintramedullary AVM (lesions of the spinal conus medul-

laris), only cutting them off from the blood flow wasinvolved.

Actual results were estimated when the patients weredischarged from the hospital. The duration of follow-upobservations varied from 4 months to 8.2 years. As shownin Table 3, in 32 patients there was a considerabledecrease or complete resolution of clinical symptomsimmediately after the operation (Type I group), in 43 therewas partial symptomatic relief (Type II group), in 10 thesymptoms did not change essentially (Type III group), andin six the neurological symptoms were aggravated (TypeIV group).

In the follow-up period, no aggravation of the neuro-logical symptoms was noted. Among the six patients inthe Type IV category, in two the neurological disordersreached the preoperative level, and in the other four, fur-ther slow resolution of symptoms was noted. Among the10 patients in the Type III group, in the follow-up periodrelief of previous symptoms was noted in eight, and in twothere was no change. Among the 43 patients in the Type IIgroup, a further decrease of symptoms was noted in 27,and among the 32 patients in the Type I group, furtherrelief of symptoms was noted in 19.

Discussion

Early classifications of spinal vascular processesincluded tumors and tumor-like diseases, such as heman-gioblastomas and hemangiomas.3 In 1987, Rosenblum, etal.,18 offered an up-to-date classification of spinal vascularmalformations based on the data acquired during exami-nation and treatment of 81 patients. These authors dividedspinal AVMs into malformations and fistulas, and they



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FIG. 8. Selective spinal angiography studies demonstrating a perimedullary AVM at the T10–L2 level. A: Contrast-enhanced segmental T-10 artery coursing from the left. B: Contrast-enhanced segmental T-12 artery coursing from theleft. 1 = feeding posterior radiculomedullary T-10 (A) or T-12 (B) artery; 2 = draining rostral vein; 3 = draining caudalvein; 4 = vascular perimedullary conglomerate of the AVM. C: Contrast-enhanced L-1 segmental artery coursing fromthe left. 1 = long ascending feeding posterior L-1 radiculomedullary artery; 2 = vascular perimedullary conglomerate; 3= segmental L-1 artery.


distinguished intradural and dural vascular malforma-tions. Intradural malformations were subdivided into in-tramedullary (glomus and juvenile AVMs) and extrame-dullary AVFs. These authors designated as dural AVFs themalformations that were situated in the dura mater andhad retrograde drainage into the perimedullary veins.

In 1997 Bao and Ling2 distinguished intramedullaryAVM, intradural AVF, dural AVF, paravertebral AVM, andCobb syndrome (metameric localization of AVM) amongthe types of malformations. Intramedullary processeswere subdivided into intramedullary and juvenile AVMs.Intradural AVFs were subdivided into Types I, II, and III,according to the intensity of the blood flow and the num-ber of tributaries. These authors supposed that, for an ade-quate choice of treatment tactics with spinal AVMs, it wasnot enough to classify the lesions according to the previ-ously established groups; it was necessary to take into

account the data about the localization and structure of aspecific malformation.

In 1995 Borden and colleagues4 subdivided spinal duralAVFs into three types by analogy with cranial dural AVFs:Type I, which had antegrade drainage into the epiduralveins; Type II, which had both retrograde (into the peri-medullary veins) and antegrade (into the epidural veins)drainage; and Type III, which had retrograde drainage intothe perimedullary veins. In our observations, however,there were no malformations that had both antegrade andretrograde drainage.

Rodesch, et al.,17 divided all spinal arteriovenous anom-alies into AVMs or AVFs, with the latter classified aseither micro- or macrofistulas. All of them correspondedto three categories, as follows: 1) genetic hereditarylesions (macrofistulas and hereditary hemorrhagic telang-iectasia); 2) genetic nonhereditary lesions (all of which



FIG. 9. Angiograms demonstrating a perimedullary AVF of the cervical spine. A: Blood is supplied by the VAcoursing from the right. B: Blood is supplied by the VA coursing from the left. 1 = radiculomedullary artery; 2 = per-imedullary veins (A) or aneurysm (B); 3 = perimedullary veins. C and D: Angiograms demonstrating a large venousbag (1), which is drained rostrally (2). E and F: Angiograms demonstrating blood drainage rostrally (1) through the pon-tomesencephalic vein (2) and into the sinus rectus (3). G and H: Angiograms obtained after the AVF occlusion.


were multiple lesions with metameric or myelomericassociations); and 3) single lesions (which could representincomplete presentations of one of the previous groups).According to these authors’ data, 81% were single lesionsand 19% were multiple; among these, 59% were trueintradural shunts with metameric features. Ten cases ofCobb syndrome, three of Klippel–Trenaunay syndrome,and two of Parkes–Weber syndrome, all with associatedspinal cord lesions, were observed. Nineteen percent of allmalformations were fistulas; 23% of those were macrofis-tulas, of which 83% were related to Rendu–Osler–Weberdisease.17

In 2002, Spetzler, et al.,19 offered a new classification ofspinal vascular processes. Among these entities theauthors distinguished the following: spinal tumor vascularprocesses (hemangioblastomas, cavernous malforma-tions), spinal aneurysms, AVFs, and AVMs. Among theAVFs they distinguished extradural and intradural lesions,with the following subclassifications: for ventral loca-tions, A designated insignificant blood shunting, B wasfor moderate shunting, and C meant considerable shunt-ing; for dorsal locations, A meant one tributary and B des-ignated lesions with numerous tributaries. Among AVMs



11

FIG. 11. Selective spinal angiography.A–C: Angiograms demonstrating a per-imedullary AVF with a blood supply from theanterior spinal artery at the L1–2 level. The ante-rior spinal artery receives its main inflow fromthe anterior radiculomedullary artery at the T-11level (the artery of Adamkiewicz). D–F:Angiograms demonstrating that the fistula hasbeen cut off at the L-1 level by clips placed atthe site where the anterior spinal artery emptiedinto the perimedullary vein. (Clips are designat-ed by the arrows.)

FIG. 10. Intraoperative photographs. A: Perimedullary veinsbefore occlusion of the fistula. B: Status during occlusion.Retrograde blood flow from the veins of the posterior fossa wasblocked by clips.


these authors distinguished extradural–intradural,intradural, and intramedullary lesions (compact, diffuse,or spinal cord conus). Intramedullary diffuse AVMs,5,6

which had been described earlier but were nowhere clas-sified, as well as the first AVM distinguished in the spinalcord conus, were added to the classification.

From our point of view, the choice of surgical treatmentdepends on the localization, structure of the vascular net-work, and hemodynamic peculiarities of the AVM.Lengthwise (according to vertebral level) and axial (theanatomical relationship to the spinal cord) localization arethe most important characteristics of a malformation. Thetypes of feeding and draining vessels will depend on theaxial and lengthwise localization because the blood sup-ply to a malformation is always provided by the vesselspassing nearby. The second most important characteristicis the structural type of malformation (AVF or AVM), tak-ing into account compact or diffuse arrangement of thenidus vessels. The number of feeding vessels and the vol-ume of blood flow depend on the dimensions of the AVMor AVF. We divided malformations into the following cat-egories according to their axial localization: intramedul-lary, perimedullary, dural, epidural, intravertebral, or com-bined. In accordance with the hemodynamic data, threetypes of blood flow (A, B, or C) were distinguished in themalformations. To simplify the classification, we considerit necessary to indicate first the axial localization of themalformation and its structural peculiarities, and then therest of its features (lengthwise localization, the type ofinflow and outflow, and the intensity of blood flow)should be indicated as supplementary to the malforma-tion’s characteristics.

We added the following new types of malformations tothe proposed classification: the intramedullary diffuseAVM described earlier;15 the intradural perimedullaryAVM described by Miyamoto, et al.,11 and also found inour observations; and the dural AVM, epidural AVM andAVF, and an intervertebral AVM discovered in our clini-cal material. Epidural AVFs were described earlier byAsai, et al.1 We observed intramedullary AVMs of theconus medullaris, as did Spetzler, et al.,19 but in our obser-

vations there were also perimedullary AVFs, which weresituated in the conus region and received inflow from thearteries passing among the cauda equina. These cases aredefined in our classification as correspondingly intra-medullary or perimedullary AVM/AVFs with lengthwiselocalization in the conus medullaris. To classify per-imedullary AVFs, we defined the following types: 1) so-called vertebral fistulas described earlier;1,8 2) per-imedullary AVFs localized in the thoracic spine; and 3)perimedullary AVFs occurring as lesions in the conusmedullaris that were discovered in our clinical material, asperimedullary AVFs localized at 1) the cervical, 2) tho-racic, and 3) conus medullaris regions, respectively. Thefistulas that receive their blood supply from the VAs arealso dissimilar; “low” and “high” AVFs are distinguishedamong them in the literature. The “high” vertebral fistulasreceive inflow directly from the VAs, but they drain firstinto the veins accompanying the VA and then into theepidural veins.1,8 Therefore, they are mostly epiduralAVFs, as opposed to “low” vertebral fistulas that drainthrough the radiculomedullary artery to perimedullaryveins.19

The division of spinal vascular malformations accord-ing to their localization and structural and hemodynamicprinciples favored the working out of a clear algorithm oftreatment for these malformations.

For the intramedullary spinal AVM, endovascular aswell as microsurgical interventions can be applied.However, endovascular treatment is not always safe, it isoften impossible to cut off all the feeding vessels with thismethod, and the intramedullary nidus volume remains thesame after treatment.3 Nevertheless, in 8% of observationsSpetzler and coauthors19 failed to resect intramedullaryAVMs completely. Therefore, in those authors’ opinion,when there is a considerable blood flow in an AVM, it isnecessary to embolize it first and then resect it microsur-gically. We used the same surgical principles:intramedullary AVMs with low and medium blood flowwere treated microsurgically, whereas AVMs with a pro-nounced blood flow were embolized first and then resect-ed microsurgically.



FIG. 13. Intraoperative photograph showing the angiographical-ly occult perimedullary AVF of the conus medullaris. The radicu-lomedullary artery, which passes with cauda equina roots inflow-ing into the large perimedullary vein, is the feeding vessel. C =caudal pole of the surgical wound; R = rostral pole of the wound.

FIG. 12. Intraoperative photograph showing the lateralapproach, and a clip placed on the anterior spinal artery at the pointof its inflow into the perimedullary veins.


Perimedullary AVFs may be treated microsurgically orembolized, or a combination of the two methods may beused.5,7,10 When they are embolized, however, there is agreat probability of recurrence, and the frequency of com-plications is high. On the other hand, if a microsurgicaltechnique is used, the frequency of complications is lowerand the efficacy of intervention is higher.5 At present,many authors prefer to treat perimedullary AVFs with lowblood flow microsurgically, but to embolize AVFs with

pronounced blood flow.7,10,14,16 Taking into account the factthat perimedullary AVMs consist of a conglomeration ofvessels and often have several tributaries, only microsur-gical interventions should be applied. During the opera-tion we were trying to achieve radical removal of theAVM and to be sure to preserve the spinal arteries.

With dural AVMs and AVFs, microsurgical as well asendovascular intervention is possible.21 The relative sim-plicity of implementation and absence of complications



13

FIG. 14. Neuroimages demonstrating dural AVM with perimedullary venous drainage. A and B: Preoperative MRimages. Expanded perimedullary veins around the spinal cord are indicated by the arrows. C–E: Selective spinalangiography of the T-10 segmental artery coursing from the right; panels D and E demonstrate drainage through the per-imedullary veins. F: Angiogram demonstrating AVM status after endovascular occlusion of the radiculomeningealartery. The point of the occlusion is indicated by the arrow; the malformation has been completely cut off. G–I:Postoperative MR images obtained after surgical occlusion of the AVM. The spinal cord edema remains, but the expand-ed perimedullary veins are not visualized. 1 = segmental artery; 2 = radiculomeningeal artery; 3 = microconglomerate ofthe AVM; 4 = radicular vein; 5 = perimedullary veins.


with the use of endovascular techniques in cases of duralAVM and AVF is attractive.10,20 Meanwhile, even if thefollow-up angiographic study demonstrates that theendovascular intervention has been performed with com-plete success, recurrences appear in a number of cases.These may be caused by a good collateral blood flow inthe dura mater. In our case of a dural AVF with retrogradeperimedullary drainage, endovascular embolization wasperformed with complete obliteration of the fistula, andour follow-up evaluation was based on angiographicallyobtained data. A lack of clinical effect after the operationimpelled us to perform an MR imaging study whichdemonstrated, as before, expanded perimedullary veins. Amicrosurgical intervention was then performed, duringwhich arterialized perimedullary veins were found. Theocclusion of the radicular vein draining blood from the fis-tula into the perimedullary veins resulted in cessation ofarterialization of the perimedullary veins, which was laterconfirmed by the repeated MR imaging data. Finally, clin-ical improvement ensued.

With dural AVMs and AVFs there is a method used tosearch for the location of the fistula or AVM in the duramater. However, it requires the resection of the interverte-



FIG. 16. Angiograms revealing an AVF in the VA, which is mainly drained by the epidural veins. A and B: Directprojections. C and D: Lateral projections. E and F: Balloon occlusion of the VA supplying blood to the lesion. Gand H: Angiograms demonstrating retrograde blood flow into the AVF from the opposite VA after occlusion of the VAsupplying blood to the lesion and the fall of pressure in the AVF. 1 = VA; 2 = draining epidural veins; 3 = balloon usedin occlusion; 4 = AVF with retrograde filling.

FIG. 15. Intraoperative photographs. A: Arterialized per-imedullary veins are depicted. The retrograde draining radicularvein is lifted slightly with a hook. B: After the coagulation andocclusion of the dorsal radicular vein (shown being lifted), arteri-alization of the perimedullary veins has ceased, and the veins haveturned blue and have become flat.




15

FIG. 17. Preoperative MR images demonstrating an intravertebral glomus AVM with extravertebral spreading.

FIG. 18. Preoperative MR image and angiograms demonstrating a combined, mainly intradural glomus AVM at theT9–11 level, with its blood supply arising mainly from the radiculomedullary arteries. A: Preoperative MR imageacquired in a T2-weighted sequence. B: Selective spinal angiography studies of the segmental artery, T-10 level, cours-ing from the left, early arterial phase. 1 = spinal branch, which passes into the posterior radiculomedullary artery; 2 =intramedullary/perimedullary AVM conglomerate; 3 = perimedullary draining veins; 4 = radiculomeningeal arteries; 5 =dural vascular conglomerate. C: Angiogram obtained in the final arterial phase. 1 = vessels of the intramedullary/per-imedullary conglomerate; 2 = vessels of the dural conglomerate; 3 = perimedullary draining veins. D: Left injection ofthe T-9 segmental artery. The vascular conglomerate (2) is fed by the posterior radiculomedullary artery (1). E:Angiogram of the T-11 level of the segmental artery from the left. 1 = epidural conglomerate; 2 = draining epidural veins.


bral joint to be wide enough, which is often accompaniedby postoperative radiculopathy. We prefer to cut off theradicular draining vein. This technique provides goodclinical results and the recurrence of AVF/AVM has neverbeen seen.

Different authors recommend endovascular as well asmicrosurgical treatment of epidural AVMs and AVFs inaccordance with the volume of blood flow and the size ofthe feeding and draining vessels. With VA fistulas thathave epidural drainage, endovascular occlusion is an opti-mum method.19 Epidural AVMs and AVFs in the thoracicand lumbar spines are better treated microsurgically, espe-cially if they are situated in the artery of Adamkiewiczregion.

With intravertebral AVMs, we combine embolizationwith a subsequent open operation. If necessary, intraoper-ative vertebroplasty is applied. Unless there is compres-sion of nerve structures, we recommend applying endo-vascular embolization and/or transcutaneous vertebro-plasty with bone cement. As a rule, combined AVMsrequire endovascular embolization followed by partial orcomplete resection of the malformation and decompres-sion of the spinal cord.2,3,6,19,21



TABLE 2Methods of treatment used in 91 patients with AVMs

Interventions

Axial Localization Structural Features of Lesion Endovascular Microsurgical Combined Total

I. intramedullary 1. glomus or compact 2 16 3 212. diffuse 0 9 0 9

II. intradural or perimedullary 1. glomus AVM 1 3 0 42. AVF 5 9 1 15

III. dural 1. glomus AVM 1 4 0 52. AVF 2 25 1 28

IV. epidural 1. glomus AVM 0 2 0 22. AVF 0 1 0 1

V. intravertebral 1. glomus AVM limited by vertebra 0 1 0 12. glomus AVM w/ paravertebral spreading 0 0 1 1

VI. combined 1. mainly intradural glomus AVM 1 0 2 32. mainly extradural glomus AVM 1 0 0 1

total 13 70 8 91

TABLE 3Results of surgical treatment in 91 patients with AVMs

Treatment Results*

Axial Localization Structural Features of Lesions I II III IV Total

I. intramedullary 1. glomus or compact 7 10 3 1 212. diffuse 4 5 0 0 9

II. intradural or perimedullary 1. glomus AVM 4 0 0 0 42. AVF 3 6 4 2 15

III. dural 1. glomus AVM 0 5 0 0 52. AVF 11 12 2 3 28

IV. epidural 1. glomus AVM 1 1 0 0 22. AVF 0 1 0 0 1

V. intravertebral 1. glomus AVM limited by vertebra 0 1 0 0 12. glomus AVM w/ paravertebral spreading 0 1 0 0 1

VI. combined 1. mainly intradural glomus AVM 1 1 1 0 32. mainly extradural glomus AVM 1 0 0 0 1

total 32 43 10 6 91

* Roman numerals denote the following results: I, considerable or complete resolution of neurological symptoms; II, improvementof symptoms; III, no changes; IV, aggravation of symptoms.

FIG. 19. Intraoperative photograph of a combined glomusAVM. A: Dura mater is pierced by arterial vessels. B:Periintramedullary vascular conglomerate is depicted.


Conclusions

For a successful surgical treatment of spinal AVMs, it isnecessary to obtain as complete a set of data as possibleabout their localization, vascular structure, and hemody-namics. This information will promote the use of optimumsurgical methods and the latest microsurgical andendovascular interventions, with treatments differentiatedaccording to the type of malformation. One should try toapply the least invasive endovascular approach in thesecases, where possible, to occlude the AVM or to reducethe intensity of blood flow by embolization. When per-forming an AVM resection or occlusion, one should use adirect approach to the malformation, blocking only thevessels supplying blood to the malformation and preserv-ing the ones feeding the spinal cord. It is necessary toresect the AVM nidus sharply only along the border withthe spinal cord. After the operation, it is always necessaryto obtain an MR image and a selective spinal angiographystudy for follow-up evaluation. Only such a combinationof neuroimaging methods can identify the remnants of apathological vascular formation.2,3,19

References

1. Asai J, Hayashi T, Fujimoto T, et al: Exclusively epidural arte-riovenous fistula in the cervical spine with spinal cord symp-toms: case report. Neurosurgery 48:1372–1376, 2001

2. Bao YH, Ling F: Classification and therapeutic modalities ofspinal vascular malformations in 80 patients. Neurosurgery40:75–81, 1997

3. Barrow DL, Awad IA (eds): Conceptual overview and manage-ment strategies, in Spinal Vascular Malformations. ParkRidge, IL: The American Association of NeurologicalSurgeons, 1999, pp 169–180

4. Borden JA, Wu JK, Shucart WA: A proposed classification forspinal and cranial dural arteriovenous fistulous malformationsand implications for treatment. J Neurosurg 82:166–179, 1995

5. Cawley CM, Barrow DL: Intradural perimedullary spinal cordarteriovenous fistulas, in Barrow DL, Awad IA (eds): SpinalVascular Malformations. Park Ridge, IL: The AmericanAssociation of Neurological Surgeons, 1999, pp 147–160

6. David CA, Giancarlo VA, Zabramski JM: Juvenile and diffusespinal arteriovenous malformations, in Barrow DL, Awad IA(eds): Spinal Vascular Malformations. Park Ridge, IL: TheAmerican Association of Neurological Surgeons, pp 161–168,1999

7. Hida K, Iwasaki Y, Ushikoshi S, et al: Corporectomy: a directapproach to perimedullary arteriovenous fistulas of the anteriorcervical spinal cord. J Neurosurg 96 (2 Suppl):157–161, 2002

8. Hori Y, Goto K, Ogata N, et al: Diagnosis and endovasculartreatment of vertebral arteriovenous fistulas in neurofibromato-sis Type 1. Intervent Neuroradiol 6:239–250, 2000

9. Krings T, Mull M, Gilsbach JM, et al: Spinal vascular malfor-mations. Eur Radiol 15:267–278, 2005

10. McDougall CG, Deshmukh VR, Fiorella DJ, et al:Endovascular techniques for vascular malformations of thespinal axis. Neurosurg Clin N Am 16:395–410, 2005

11. Miyamoto S, Hashimoto N, Nagata I, et al: [Surgical treatmentof spinal perimedullary AVF/AVM.] No Shinkei Geka 28:213–217, 2000 (Jpn)

12. Mont’Alverne F, Musacchio M, Tolentino V, et al: Giant spinalperimedullary fistula in hereditary haemorrhagic telangiectasia:diagnosis, endovascular treatment and review of the literature.Neuroradiology 45:830–836, 2003

13. Mourier KL, Gobin YP, George B, et al: Intradural per-imedullary arteriovenous fistulae: results of surgical andendovascular treatment in a series of 35 cases. Neurosurgery32:885–891, 1993

14. Nagashima C, Miyoshi A, Nagashima R, et al: Spinal giantintradural perimedullary arteriovenous fistula: clinical and neu-roradiological study in one case with review of literature. SurgNeurol 45:524–531, 1996

15. Ohata K, Takami T, El-Naggar A, et al: Posterior approach forcervical intramedullary arteriovenous malformation with dif-fuse-type nidus. Report of three cases. J Neurosurg (Spine 1)91:105–111, 1999

16. Ricolfi F, Gobin PY, Aymard A, et al: Giant perimedullary arte-riovenous fistulas of the spine: clinical and radiologic featuresand endovascular treatment. AJNR Am J Neuroradiol 18:677–687, 1997

17. Rodesch G, Hurth M, Alvarez H, et al: Classification of spinalcord arteriovenous shunts: proposal for a reappraisal—theBicêtre experience with 155 consecutive patients treatedbetween 1981 and 1999. Neurosurgery 51:374–380, 2002

18. Rosenblum B, Oldfield EH, Doppman JL, et al: Spinal arteri-ovenous malformations. A comparison of dural arteriovenousfistulas and intradural AVMs in 81 patients. J Neurosurg 67:795–802, 1987

19. Spetzler RF, Detwiler PW, Riina HA, et al: Modified classifi-cation of spinal cord vascular lesions. J Neurosurg 96 (2Suppl):145–156, 2002

20. Steinmetz MP, Chow MM, Krishnaney AA, et al: Outcomeafter the treatment of spinal dural arteriovenous fistulae: a con-temporary single-institution series and meta-analysis. Neuro-surgery 55:77–88, 2004

21. Tai PA, Tu YK, Liu HM: Surgical treatment of spinal arteri-ovenous malformations: vascular anatomy and surgical out-come. J Formos Med Assoc 100:389–396, 2001

22. Tenjin H, Kimura S, Sugawa N: Coil embolization of vertebro-vertebral arteriovenous fistula: a case report. Surg Neurol 63:80–83, 2005

Manuscript received November 30, 2005.Accepted in final form April 4, 2006.Address reprint requests to: Eugene I. Slin’ko, M.D., Ph.D., In-

stitute of Neurosurgery, Manuilsky Street 32, 04050 Kiev, Ukraine.email: [email protected].



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