LE JOURNAL CANADIEN DES SCIENCES NEUROLOGIQUES

University of Toronto Neurosurgical Rounds No. 4 Global Arteriovenous Malformation of the Cervical Region

R.C. HOLGATE and W.M. LOUGHEED

INTRODUCTION tent low back pain and sciatica. The This case was presented as an physical findings were marked nuchal interesting example of a global arterio­ spasm, limitation of neck movements, lumbar muscle spasm, and straight leg venous malformation (AVM) involving raising on the right limited to 45 degrees. muscle, bone, extradural and intra­ Treatment consisted of bed rest and dural spaces of the cervical region. lumbar traction. Improvement occurred and he was discharged with his neck brace. CASE HISTORY Eight months later a third admission was necessary because of a sudden onset of A twenty-eight year old male in October, headache and vomiting. There were no 1976, fell at work sustaining a blow to his focal neurologic signs, but his neck was lower back. The following day he com­ stiff. A lumbar puncture revealed bloody plained of cervical pain. Physical examina­ spinal fluid. A CT scan showed slight tion was negative and he had a full range of ventricular enlargement. Cerebral angio­ movement of his cervical spine. grams were normal. Plain films and tomograms of the cervical spine showed a lytic honeycomb After much deliberation it was concluded lesion of C2 and C3, and a 4 mm. that in spite of the risks involved an subluxation of C3 on C4 (Fig. 1). The bone attempt at embolization should be made. scan showed increased flow and decreased Via a right transfemoral catheter the left static activity in the upper cervical region. ascending cervical was embolized The radiological diagnosis was vertebral with a mixture of gelfoam and pantopaque hemangioma; tumor, infection and histio­ (Fig. 7). This reduced considerably the cytosis were unlikely but important abnormal vasculature. The right occipital differential considerations. and ascending pharangeal were The lesion was further evaluated by catheterized. There was a large aneurysm myelography which showed a circumferen­ arising off the right ascending pharangeal tial narrowing of the subarachnoid space artery. After embolization this aneurysm without actual cord compression from C4 was occluded and the vascular shunt much to the foramen magnum (Fig. 2). Angio­ reduced (Figs. 8 and 9). graphy revealed an extensive angiomatous After the procedure the patient com­ mass in the vertebral bodies and posterior plained of retrobulbar pain and that he elements of C2 and C3 with a large could not see properly. Examination extradural collection of abnormal vessels proved that with effort he could read and in the spinal canal. An intradural com­ that his vision was 20/30 in both eyes. He ponent was not detected and the anterior stated that the print was blurred. Fundi spinal artery was not identified. The lesion were normal and visual fields, although received blood supply from the vertebral difficult to assess, were probably normal. arteries, ascending and deep cervical He showed a loss of convergence and arteries, and the ascending pharyngeal paralysis (UMN) of the left arm and leg artery bilaterally. Muscular branches of with incoordination. Eight days later the these vessels, as well as the occipital arm and leg weakness had improved. There arteries, were linked by direct arterial was nystagmus in all direction of gaze, anastomosis to each other providing upward gaze was limited and pupillary alternate routes of supply (Figs. 3, 4, 5 and reaction only moderately brisk to light. He 6). had suffered a mid brain lesion resulting in Because of the complexity of the a Parinaud's syndrome. By the time of From the Department of Radiology. Toronto malformation it was decided to treat the discharge all findings had cleared. From General Hospital. University of Toronto, and the the above complication the emboli must Division of Neurosurgery. Toronto General Hospital, patient conservatively. He was fitted with a University of Toronto. neck brace and discharged. have reached the vertebral system from the Between his first admission in 1976 and muscular branches. Reprint requests to Dr. W.M. I.ougheed. Division of Neurosurgery. Toronto General Hospital. 101 College his second admission in March, 1978, the On February 26, 1980, he was carrying Street. Toronto. Ontario. Canada M5G 1 L7. patient continued to suffer from intermit­ his child upstairs on his shoulders when he

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in muscle, bone, extradural, intradural and intramedullary sites. The extradural AVM's form about 15-20% of all vascular spinal abnor­ malities according to Bischof (1967). Feeders to the extradural malforma­ tions usually do not have any com­ munications to the arteries feeding the spinal cord. However, Kendall and Logue (1977) reported one case draining to the intrathecal . The extradural AVM's are much less common in the cervical region, the most common site being mid thoracic. According to Pia (1978), 27% show an apoplectiform course, 42% a a b remitting course, and 31% a progressive course. Figure 3 — A and B — Right and left Extradural hemorrhage or mass vertebral angiogram. Subtracted views effect produces spinal cord compres­ of the injections show Figure 1 — Lateral view of the cervical extensive collections of abnormal vessels sion with serious consequences. When spine. There is a minor forward in the upper four vertebrae (right more the vertebral body is involved patho­ subluxation of C2 and C3. The bone than left). Lateral views confirmed the logical fracture may occur. texture of C2 and C3 is abnormal intraosseous position. Because of the partial block in the showing the typical honeycomb appear­ myelogram it would appear that in the ance of a vertebral hemangioma. On admission, examination was normal future this patient will suffer from except for limitation of neck movements. spinal cord compression. Pia (1978), While in hospital the patient stated he stated that the timing for extradural could no longer hear the bruit. We had AVM's to cause compression was 2-4 never heard a bruit, which had been years following diagnosis. He made a complained of on admission, and there was plea for early treatment before a fixed no bruit audible on this examination. The neurologic deficit. Decompression patient was again discharged having would require laminectomy and extra­ improved. dural cauterization of the feeding vessels to the extradural component. The difficulty in staging the procedures DISCUSSION becomes apparent as the muscular part Dr. W.M. Lougheed of the malformation feeds the extra­ The vascular supply to the nuchal dural component and hemostasis may muscles and vertebral bodies, extra­ be extremely difficult if the muscular dural space and spinal cord is outlined component is not occluded first. in Figure 11 (Pia and Djindjian, 1978). Unfortunately, we cannot surgically The ascending cervical and deep remove the muscular component due cervical arteries anastomose with both to the extent and the anatomy, and the spinal cord circulation and vertebral embolization is not possible without arteries. In turn, the vertebral artery first separating the extradural and contributed to the spinal cord circula­ intradural components. The only tion and with the external carotid certain way of accomplishing this would be to occlude all the radicular Figure 2 — Lateral view of the cervical circulation via the . The occipital artery also anastomoses with arteries coming from the vertebral and myelogram. There is a circumferential ascending cervical branches. This, narrowing of the dural sac (seen best the deep cervical. Due to the extensive anteriorly) which extends from C4 to network of communicating arteries however, might compromise the normal the foramen magnum. each of these systems can therefore blood supply to the spinal cord. The take part in the supply to the AVM vertebral component might be elimi­ making total irradication a complex nated by ligation of both vertebrals sneezed. This resulted in a sudden severe intradurally. This would have to be pain in his neck. The patient had noted in problem. Figure 12 (Pia and Djindjian, 1978), staged, necessitating two exposures. the last few months that every time he The proximal portion of the vertebral sneezed, coughed or strained he had to nicely illustrates the complex arrange­ hold his head between his hands to prevent ments which may occur, especially arteries could be embolized with large severe neck pain. when the AVM is global and is located emboli. If the emboli were small there

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a Figure 4 — A and B — Deep cervical artery. Selective injections Figure 5 — A and B — Selective ascending cervical angiogram. into the deep cervical arteries show enlargement and tortuosity The ascending cervical arteries also show hypertrophy (more of the parent vessels and numerous abnormal vessels in the marked on the right) A.) and supply of abnormal vessels to both posterior elements and soft tissues. Of interest, an aneurysm can the vertebral bodies and surrounding soft tissues. be identified on the left (B) (arrowhead), and direct anastomoses to the vertebral artery (arrowheads) can be seen on the right (A).

Figure 6 — Left external carotid injections. The left ascending Figure 7 — Embolization, left ascending cervical artery. The pharyngeal artery (A) and the left occipital artery (B) also give catheter is well seated in the ascending cervical artery (A- direct and anastomotic supply to the hemangioma. Similar arrowhead). Following embolization (A-B) there is obliteration pictures were obtained on the right. of the parent vessel and a reduction in the flow to the malformation (compare with Fig. 5B). Despite good placement of the catheter a complication occurred as outlined in the text, presumably via the direct arterial-arterial anastomoses to the vertebral artery (B-arrowheads).

would be danger of embolizing normal to obstruct the vertebral intradurally infarct as he had previously. Perhaps, cord circulation. Perhaps safer, but of and then follow with proximal embo­ if the emboli were large enough this more complexity would be to use a lization. The sides could then be could be avoided. graft from the subclavian to the staged. We did not visualize any intradural intradural segment of the vertebral I am still perplexed as to how to deal component by selective cord angio­ artery and tie off the other vertebral with the ascending cervical branches graphy. However, in the post emboliz­ intradurally. This would be carried out because they give many branches to ation angiogram the anterior spinal at the time of laminectomy. A third the spinal cord and embolization artery became visible and no angioma solution might be cannulation of the would probably result in a spinal cord was seen. Since the patient clearly had vertebral artery with a catheter balloon infarct this time instead of a brain stem a subarachnoid hemorrhage we must

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assume that he has either a small intervention. Dr. Holgate has consented intradural AVM or that he bled from to discuss intra-arterial embolization the intradural veins draining the (IAE). malformation. Only one case has been reported of an extradural AVM Dr. R.C. Holgate draining via the intradural veins Complete removal of the shunt is the (Logue, 1977). most definitive treatment of arterio­ Stabilization of the cervical spine venous communications. In this case, should be considered eventually because because so much of the shunt occurs he already has some subluxation and within the bone of three consecutive vertebral body collapse or fracture is vertebrae, surgical removal is impos­ one of the complications of intraosseous sible. extradural AVM's. Posterior fusion An alternative to removal of a shunt would be better but how to time this is to occlude it either by inducing with all the other procedures is thrombosis or by obliterating, and/or difficult. If a bypass graft is in place obturating it with biologically com­ then posterior fusion would be unde­ patible materials or devices — intra­ sirable for fear of graft failure. arterial embolization (IAE). Figure 9 — Post embolization plain film. Anterior fusion might be difficult Materials, devices, and methodology The plain film following embolization shows the distribution of the pantopaque unless the extraosseous component exist by which any vessel in the body can be dealt with first. labelled Gelfoam. Note the large can be successfully occluded. The collection in the ascending pharyngeal I have decided to do nothing until hazard of IAE rests not with its ability aneurysm (arrowhead). his clinical state clearly demands to successfully occlude the target vessel,

Figure 8 — A and B — Right external carotid embolization. Figure 10 — A and B — Follow-up angiography. During his A. Before embolization a large aneurysm (arrowheads) of the third admission a late post embolization angiogram was done. ascending pharyngeal artery and intraosseous supply to the In Fig. 10A the previously obscured upper is seen. B. After embolization the (arrowhead) can now be identified against the background of aneurysm is obliterated and the intraosseous vessels no longer reduced left ascending cervical supply. The supply from the opacify. unembolized left vertebral artery has increased its contribution.

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but with its inability to avoid the picture of the natural history of the occlusion of other vessels not part of lesion, knowledge that a co-existing the target. Assessment of the risk of intra-axial component may be present IAE is an estimation of the relative and untreated and, no assurance that chance and the degree of dysfunction further subarachnoid haemorrhage which might attend the inadvertent (the mechanism is uncertain) would be occlusion of the off target vessels. prevented. In this case there is global contribution The therapeutic alternatives are: 1) and perhaps more importantly inter­ palliative management of the compli­ communication between all of the cations as they occur, and 2) evaluation vessels in the geographic area (vertebral, of the patient's fibrinolytic mechanisms thyrocervical, costocervical and ex­ to rule out the possibility of medical ternal carotid). As a consequence, therapy. although the majority of emboli released into any of these vessels will Dr. A.R. Hudson be drawn by sump effect into the shunt Dr. Hoffman would you consider an irreducible minimum will be radiation therapy in this case? directed hemodynamically into the spinal cord, brainstem and higher Dr. H. Hoffman centers. X-ray therapy for arteriovenous The problem then reduces itself into malformation has been advocated for how to isolate the neural tissue from many years. Although there have been the hemangioma (accepting the fact sporadic reports of obliteration of an that one cannot be certain that none of AVM by conventional radiotherapy, the lesion is intra-axial). most reports using this therapy have There is probably no role for IAE in not been studied angiographically and this case unless definitive therapy is so the presumed beneficial effect of the anticipated. Definitive therapy would radiation has not been proven. Further­ Figure II — The vascular supply of the be aimed at: a) removing/obliterating more, there is a very definite danger of cervical region from Pia and Djindjian the shunt; b) removing the extradural conventional radiotherapy in this (1978). mass; c) restabilizing the cervical' disorder producing radiation necrosis. spine. In his recent review of cerebral A plan of approach would have to AVM's, Drake (1979) refers to stereo­ include ligation of both vertebral tactic radiation as described by Steiner arteries just proximal to the posterior with cobalt rods and as described by inferior (PICA) origin, Kjelberg using the bragg peak of the probably in conjunction with an proton beam in an effort to obliterate attempt to establish a new posterior deeply placed inoperable AVM's. Both fossa blood supply. Following this these forms of radiotherapy resulted in procedure all the feeding vessels except complete obliteration of some AVM's, the left ascending cervical (which gives but these therapies were not completely rise to the anterior spinal artery) would free of the risk of radionecrosis. be embolized (Fig. 10). If one were to Recently, Epstein (1980) reported do IAE one would have to accept the on the beneficial effects of proton risk and less devastating disabilities beam irradiation for deeply placed attendant upon dorsolateral spinal inoperable AVM's which were not artery occlusion. The avascular angio­ amenable to embolotherapy. In his matous vertebral bodies would have to report, Epstein described cases in be removed and the cervical spine which deeply placed AVM's were fused. The surgery would be done in completely obliterated by proton beam the face of an unembolized left irradiation. ascending cervical artery. Consideration should therefore be The attempt at definitive therapy given to the possible use of stereotactic would take place in a young otherwise radiation with the proton beam in this healthy man with no neurological case if embolotherapy proves unsuc­ deficit. The risks of dorsolateral spinal cessful. artery occlusion(s) and bleeding from Figure 12 — Global arteriovenous mal­ the unembolized vessels would have to Dr. J. F. R. Fleming formation from Pia and Djindjian be accepted. Furthermore, the treat­ Dr. Lougheed, have you considered (1978). ment would occur without a clear using cardiac arrest with an injection

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of a fast setting glue to prevent it being stage, particularly as the patient is The devices enjoy effective use as swept into the neuraxis? asymptomatic. Presumably external intravascular ligatures in vascular spinal support has been provided, and tumors which are immediately removed Dr. Lougheed in my view may be the only therapeutic surgically. Because of the short time aid required. interval between IAE and surgery I would be concerned that our there is little chance of recruitment by control of the direction and extent of the tumor of collateral supply and the spread might be inadequate. Also, I Dr. Hudson usual peroperative blood loss can be suspect that this malformation has Dr. Holgate could you review for us significantly reduced. These emboli more than one nidus so the glue might the present status of embolic techniques? are also of significant value in the pass from one nidus to the other management of arteriovenous fistulae through normal intervening tissue. Dr. Holgate where a balloon may be inflated and The following section is meant to detached (or tethered proximally) to give the reader an overview of the Dr. Hudson occlude the shunt. Guide wire lengths technology available, the advantages Dr. Humphreys you have just can similarly be placed so that both the and disadvantages of each class of reviewed your experience at the afferent and efferent arterial loops of embolus. Lastly, there is a question­ Hospital for Sick Children, can we the fistula are occluded. have your comments? naire which reviews the mental hurdles encountered in assessing the advisability Despite their efficacy in the instances outlined above the devices have certain Dr. R.P. Humphreys of embolizing a particular lesion. The case reviewed in this paper will serve as limitations. Because of their finite size We have just finished reviewing our an example of the complexity of they can only be used to occlude larger experience with spinal cord arterio­ treatment planning in IAE. vessels and are not useful in the venous malformations at the Hospital nonsurgical management of tumors. for Sick Children (Humphreys, in In the management of AVM's they can print). These malformations are most CLASSIFICATION OF EMBOLI be used to isolate the lesions by commonly of the Type 111 (juvenile), 1. Embolic Devices pruning off some of the usual with lush communications, multiple Guide wire fragments, coils, bal­ collaterals and, as a secondary benefit, feeders and, in four instances, aneur­ loon catheters, detatchable bal­ increase the flow rate through the main ysmal dilatations of component struc­ loons. feeding vessels for subsequent flow- tures (Scarff, 1979). However, all of 2. Particulate Emboli directed emboli. Furthermore, the these lesions were intra-arachnoid, Blood clot (autologuos, amicar) balloons may collapse and the metallic and in part or entirely intramedullary. Hemostatic agents: Gelfoam, Sur­ devices might erode through the There was none which had the gical, microfibrillary collagen occluded vessel in time. extensive, multi-tissue involvement as Muscle Dr. Lougheed's patient. Hemoclip — Gelfoam In addition, we have had recent Polyvinyl alcohol sponge 2. Particulate Emboli experience with two children who Molybdenum beads, lead pellets, These emboli are usually released presented with extraosseous cervical iron filings into the blood stream and directed to vascular malformations. Both were Plastics: silicone spheres, poly- the lesion by its higher blood flow rate. obliterated by embolization techniques, urethane spheres The delivery system sets the stage for a procedure successful no doubt 3. Liquid Emboli the high incidence of off target emboli. because each lay within the territory of Pharmacologic agents ie: cytotoxic The catheters have large lumens to the appropriate drugs, amicar accommodate the size of the particles only. that must pass through. Sclerosing solutions ie: 50% glucose The operative approach to this Liquid plastics: acrylic tissues The tip of the catheter is often patient would be overwhelming by adhesives, liquid silicone, ferro­ placed in a proximal position ie: virtue of the lush vascular supply magnetic silicone. cervical for a beginning presumably within para­ middle cerebral AVM. The emboli are vertebral musculature, and extending released into the blood stream and the through bone to the ventral dural /. Embolic Devices larger percentage will be flow-directed surface. Even with radical operative This class of embolus is delivered or into the shunts until obliteration is well techniques, such as total circulatory placed in the vascular tree at the tip of underway. At some point the preferen­ arrest (which we have not found to be an angiographic catheter. Because of tial flow to the shunt will be reduced useful for the vein of Galen malforma­ their size (guide wire fragments, and an increasing number of emboli tions in the neonate), there is no balloons) the complexity of their shape will enter the off target area. guarantee that the anatomical exposure (coils) they remain in situ at the In the external carotid system the will allow the definition of the catheter tip and are hence, the least catheter is often more selectively ventrally situated dural lesion. likely of all emboli to give rise to placed. Furthermore, occlusion of off It is tempting therefore, to recom­ complications due to occlusion of off target vessels has less devastating mend that nothing be done at this target vessels. effects. Nevertheless, a point will be

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reached at which the shunt is partially are delivered through balloon tipped used as an adjunct/assist to sur­ occluded and the pressures used to microcatheters. These catheters are 1-2 gery? ie: if surgery is contemplated inject the emboli will transiently Fr in size opposed to the 5-9 Fr size a more limited embolization may exceed the pressure directing blood employed for devices and particulate well suffice. through the shunt. Once this imbalance emboli. 3. What tissues are exposed to obtains, flow can be reversed and The balloon tip of the catheter potential off target emboli? emboli can be propelled backwards allows for supraselective catheter 4. Can the damage (deficit) resulting through the external carotid artery placement ie: middle cerebral or from off target emboli be tolerated/ and thereby gain access to the internal . Once in place and accepted in the face of current carotid artery and the brain. Reflux of inflated the balloon will also prevent knowledge of the natural history emboli can be prevented by wedging or reflux of the occluding liquid into off of the lesion untreated? ballooning the catheter tip, but at the target vessels. 5. If the lesion is to be embolized cost of losing the preferential flow that The drawbacks of this technique are what steps can be taken to avoid directs the emboli to the lesion. inherent in the substances used. The off target emboli? Apart from the increased hazards of acrylics are less viscous and can easily 6. Are the materials and expertise stray emboli, particles have limitations produce an intravascular cast which available to perform the type of by virtue of their composition. Blood occludes both the arterial and venous embolization most efficacious for clots, and the hemostatic agents side of a shunt, but the substance is too this lesion? though safe seldom give rise to efficacious and enters not only the permanent obliteration of the occluded shunts but the normal capillary beds in REFERENCES vessels because they are rapidly surrounding tissues leading to a removed by the fibrinolytic system. greater propensity to infarction of BISCHOF, W., SCHETTLER, G. (1967): Sur Klinik und Therapie der Arteriovenosen The plastic beads (silicone, polyure- intervening normal tissue. There have Angiome und Varikosen des Ruckenmarks. thane) are more permanent but only been problems with intracerebral Dtsch. Z. Nervenheilk 192: 46-68. obturate the vessels and do not bleeding and catheters which have DRAKE, C.G. (1979): Cerebral Arteriovenous promote subsequent thrombosis. Poly­ become "glued" inside the head. Malformation; Considerations for and Ex­ vinyl alcohol sponge and muscle Liquid silicone in its normal state is perience with Surgical Treatment in 166 produce safe permanent occlusion, but cases. Clinical Neurosurgery, 26: 145-208. too viscous. Ingeniously treated, its EPSTEIN, F. (1980): Presented at the annual are limited in usefulness by technical viscosity has been greatly reduced, but meeting of American Society of Pediatric difficulties in delivering the emboli at the cost of increasing its hardening Neurosurgery. Peter Island, British Virgin into the catheter and in the preprocedure time. Because of this slow setting time, Islands. production of regularly shaped, prop­ isolation of the target vessels from the HUMPHREYS, R.P. Cerebraland Spinal Cord erly sized emboli. influx of untreated blood is a must, Arteriovenous Malformations, In Pediatric Neurosurgery: Surgery of the Developing This method of embolization is most thus increasing the technical complexity Nervous System, Ed. R.L. McLaurin et al., useful in the presurgical management of embolization and often requiring Grune and Stratton, Inc., New York (in of extremely vascular (shunt containing) that multiple catheters be employed. press). extracranial tumors and malformations. Liquid silicone is clearly the best KENDALL, B.E., LOGUE, V. (1977): Spinal Silicone spheres are the safest emboli material for the nonsurgical, stand epidural angiomatous malformation draining for intracerebral malformations but alone, embolic treatment of such into intrathecal veins. Neuroradiology 13: 181-190. their efficacy is not high ie: complete lesions as glomus jugulare tumors. It PIA, H.W., DJINDJIAN, R. in: Spinal obliteration is a virtual impossibility. may well be the best material to use in Angiomas, Advances in Diagnosis and the treatment of spinal cord AVM's. Therapy. Berlin, Heidelberg, New York; 3. Liquid Emboli Springer Verlag, 1978. These are the newest of the embolic SCARFF, T.B., REIGEL, D.H. (1979): Arterio­ CHOOSE YOUR WEAPONS venous malformation of the spinal cord in materials and the most exciting. While children. Child's Brain 5: 341-351. liquid silicone rubber and the tissue Pre-embolization Questionnaire adhesive acrylics have been available 1. Is there an acceptable therapeutic for some time, the delivery system is alternative? not widely available. These substances 2. Is embolization to stand alone or

Continued preparation of these Case Records has been made possible by a grant to the University of Toronto from Codman and Shurtleff, Division of Ethicon Sutures Ltd.

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