Neuroradiologv

Neuroradiology (1982) 22:171-180

© Springer-Verlag 1982

Review Article

Arteriovenous Malformations (AVM) of the Spinal Cord in Children A Review of 38 Cases M. C. RichC, J. Modenesi-Freitas 1, M. Djindjian 2 and J.J. Merland 1 1Departmentof Neuroradiology,Hrpital Lariboisi+re,Paris ZDepartmentof Neurosurgery,Hrpital HenryMondor,Crrteil, France

Summary. The cases of 38 children with AVM seen at the Lariboisi~re Hospital since 1962 are reviewed. The clinical picture was often of sudden onset with impairment of motor function a n d / o r subarachnoid hemorrhage. The diagnosis was usually made by myelography, but spinal arteriography is the key examination, since it confirms the diagnosis and is essential to determine the exact location of the angioma: whether it is extramedullary, intramedullary, or mixed. Angiotomography and angiomyelography with magnification are necessary to determine if the lesion is median, compact, and if it has long sulcocommissural arteries, details which have an important bearing on the prognosis. Operation should be performed as soon as possible after its feasibility has been demonstrated angiographically. But embolization with new materials has also been effective, either associated with operation or as an alternative.

Key words: Spinal AVM in children - Spinal arteriography - Angiotomography - Embolization - AVM

Angiomas of the spinal cord continue to be regarded as dreadful afflictions when found in children. Early diagnosis is rarely made because of their relative rarity, so one is almost always faced with serious permanent ischemic or hemorragic complications. Although these lesions are usually examined neuroradiologically, they remain inadequately defined before operation in most cases, so that the operations continue to be very complex [1, 14, 20]. Evaluation of the prognosis before operation should be reconsidered today for several reasons. Myelography with water-soluble media is a superb means of diagnosis which should be used whenever

there is the slightest uncertainty. In addition, magnification and angiotomography in the area of arteriography make a precise preoperative evaluation of the lesion (i. e. its topography and operability); Embolization is a very valuable preoperative step, while myelotomy and microsurgical techniques have improved the possibility of excision. It is also possible that, in the near future, CT scans will demonstrate the exact state of the spinal cord itself.

Material and Methods The study comprises 38 cases of angiomas of the spinal cord which were diagnosed and treated at Lariboisirre Hospital between 1962, the date of the first spinal arteriograms performed by R. Djindjian [4], and 1980. These serve as a basis for a general review of the condition, the circumstances behind its diagnosis and its evolution, which leads to the conclusion that, if the diagnostic methods available today are used to the maximum, effective treatment of the malformation will be accomplished. Only malformations which produced clinical signs before the age of 15 years are included in this study. The CSFwas examined in 35 patients, myelography with gas, pantopaque, or water-soluble metrizamide was performed on 21, CT scans on 2, and all 38 had either one or several spinal arteriograms. All but five of the patients received some form of treatment. The long term clinical results in most of the cases have been reported by Michel Djindjian [3], while the most recent cases will be reported in a global study in the near future. Our principal purpose at this time is to discuss the detection of the disease, the methods 0028-3940/82/0022/0171/$02.00

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Fig. 1. Composite sketches of the various types of AVMs found by radiological study and at operation [3]. Ia: median, compact malformation with long sulcocommissural arteries; I b: compact median malformation with short sulcocommissural arteries; II b: extremely diffuse lateral malformation; IIb, IIc, IHa, IIIb: AVMs associated with intra- or extramedullary, venous or arterial dilatation

> available for exploring it, and the means by which a satisfactory analysis of the lesions can be obtained before treatment [3]. Results

Clinical Signs It is necessary to emphasize the sudden onset of symptoms since acute clinical manifestations were observed in 32 of the 38 cases. Of these 32 cases, 19 had sudden impairment of motor functions, often as a result of a physical effort. This may temporarily regress, but may also become permanent after several repeated attacks. Thus, early recognition of the condition is of great importance and should occur during the first attack if possible. Subarachnoid hemorrhage was found to be associated in 8 of the 19 patients. The symptoms ressembled those of subarachnoid haemorrhage in ten cases, although some minor signs, mainly spinal pain, focused attention on the spinal cord, thus leading to the diagnosis. The symptoms were those of simple subarachnoid haemorrhage in only three cases, and it was because of the absence of CNS involvement that myelography was performed and the origin of the hemorrhage was discovered. Progressive evolution of the disease was observed in only six patients, in whom the clinical symptoms

were often misleading, i. e. incomplete transverse section of the spinal cord, or Brown-Srquard syndrome, or cauda equina manifestations. Another finding which should be mentioned is the frequent association of deep or cutaneous angiodysplasia, either metameric or not, since this was found in 13 cases (34%). These included port wine stained angiomas, Weber-Rendu-Osler disease, Klippel-Trenaunay disease, and Cobb's syndrome [6, 9].

Cerebrospinal Fluid The CSF of 35 patients was: Hemorragic 21 cases Dissociated as to protein-cellular 8 cases levels Normal 6 cases

Plain X-ray Films These disclosed osseous abnormalities in 12 cases. Except for one case of a vertebral angioma (Cobb's syndrome), most of the abnormalities appear to have been acquired, due to the presence of the malformation and the malleable properties of bones of children. For the most part they consisted of a widening (sometimes very considerable) of the vertebral canal, scalopping of the vertebral body, erosion of the pedicles facing the malformation, or kyphoscoliosis.

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Fig.2a-c. a Marked enlargment of cervical canal of young girl with cutaneous angiodysplasias of right shoulder. Since myelography seemed prohibited, cervical arteriography was then performed, b Left vertebral arteriogram showing large venous dilatation filling cervical canal. CT scan failed to demonstrate spinal cord. c AP view of left vertebral arteriogram with selective catheterization of radicular artery feeding malformation

Myelography This was performed on only 21 cases, using Pantopaque (16 cases), metrizamide (3 cases) or gas (2 cases). In 13 cases (of which 3 were with metrizamide), the typical appearance of enlarged vessels was revealed, but an enlarged spinal cord in seven others made it difficult to distinguish it from a tumor; the myelogram revealed what was considered to be a normal spinal cord in one case.

CT Scans CT scans in two cases demonstrated an enlarged spinal cord but no additional information. Nevertheless, with the technical improvements which will undoubtedly be made, it will probably become one of the techniques of the future.

Spinal Arteriography This is the important basic examination which was performed in all cases, but global aortic arteriography, which was the primary examination in nine cases, was a diagnostic success in each case. Selective arteriography was performed from the start on the other cases.

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Fig. 3. Pantopaque lumbar myelogram of AVM of cervical spinal cord with huge draining veins and associated scalloping of the cervical vertebral bodies

Fig.4. Dysplasia of a vertebral body (arrows) in a case of Cobb's syndrome (association of vertebral hemangioma and intramedullary AVM)

Location and Evolution

usually quite large, sometimes becoming so huge that they cause gross dilatation of the vertebral canal. The thoracic angiomas have the poorest prognosis, probably because of the sensivity of the spinal cord to ischemia at this level (five paraplegics out of eight cases). They are intramedullary or mixed (except for one case), and the anterior superior dorsal spinal artery was involved in all cases. Extensive zones of softened spinal cord were often found during operation, thus explaining the paraplegia and lack of improvement after treatment. The thoraeolumbar angiomas evolve quite unpredictably. They are often voluminous mixed type angiomas (extra- and intramedullary), being fed by the anterior and posterior spinal arteries at the same time. When they are located along the conus medullaris or the filum terminale, they may be completely extrame-

The location of the angiomas was: Cervical Thoracic Thoracolumbar

11 cases 28% 8 cases 21% 19 cases 51%

This classification is important in that by correlating the clinical signs with topography at the time of discovery, a relatively good prediction of their evolution can be made. The cervical angiomas seem to remain latent for a long time and permanent impairment occurs late. This is probably due to the numerous arteries feeding the spinal cord at this level. The cervical angiomas, which generally have multiple pedicules, are always intramedullary. The veins which drain them are

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Fig. 5. Associated angiodysplasia in a case of Weber-Rendu-Osler disease without localizing signs. Subarachnoid hemorrhage led to cerebral angiography which demonstrated intracerebral telangiectasia (arrow) and an associated cervical intramedullary AVM (ai~

row)

dullary (4 cases) although fed by the anterior spinal artery. Table 1 is based mostly on surgical observations since intramedullary, extramedullary, or mixed locations could not be determined from spinal angiography, except in some of the later cases where important information was obtained from angiotomography. Fig. 6. Global aortography demonstrates intramedullaryAVM in a boy of 5 years

Table 1

Intramedullaryangiomas Mixed type angiomas Extramedullary angiomas

19 12 7

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Fig.7a-e. Left vertebral arteriogram (lateral view) demonstrates cervical intramedullaryAVM fed by a long sulcocommissural artery (arrow), a routine, b magnification; c AP angiotomogram. This AVM is compact and median, good indications for surgical extirpation

We shall see below how our techniques must be improved in order to determine the exact location of the AVM more accurately. Treatment

Because of the many modifications of surgical technique which have been made during the 18-year period of this study, we shall limit our results to a statistical presentation of the different treatments performed. The introduction of myelotomy in 1970, and the surgical microscope, have transformed the methods completely [15, 18, 21]. Different techniques are included in the term e m bolization. These range from the very first attempts at embolization using Spongel which did not give a stable result, up to the most recent techniques [8, 10, Ill. Table 2 is a simple presentation of the treatments applied. It is impossible to draw any general or deft-

nite conclusions from these, although it may be interesting to note some of the figures.

Table 2

No treatment or simple laminectomy Ligation Ligation and embolization Embolization Partial excision Embolization and partial excision Total excision Embolizationand total excision

5 5 2 8 3 5 8 2

Discussion

A review of the 38 cases shows that spinal AMVs in children are a separate pathological entity characterized by [20]:

Fig.8a-c. a Large, diffuse thoracic intrameduUary AVM on right side of spinal cord. ASA supplying angioma (arrows) is linked to AVM by short sulcocommissural arteries (arrows), but b reveals perfect blood supply to ASA through arteries of conus (posterior medullary arteries), e Arteriographic control 1 year after embolization reveals complete disappearance of malformation with conservation of patency of the anterior spinal artery. The patient recovered from severe paraplegia

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sudden onset, usually with remissions, but with successive attacks (71%), occuring at the same level; frequent subarachnoid hemorrhage (55%) intramedullary or mixed location (82%) association with cutaneous and/or osseous abnormalities (73%): 13 cases of angiodysplasia and 12 bone abnormalities; spontaneous, usually grave evolution, which justifies early treatment. Objective signs were found in 29 cases whether the onset was sudden or gradual, and most often indicated injury to the spinal cord. However, when presented with subarachnoid hemorrhage with no obvious cerebral involvement one should not overlook the possibility of making X-rays of the vertebral column and myelography with watersoluble media. Three such cases were discovered with no apparent signs which pointed to the spinal cord. Myelography with watersoluble media not only makes diagnosis possible, but also enables one to appreciate the relationship between the spinal cord and the malformation. However, the potential danger involved with this sort of myelography in cases of huge angiomas should be stressed. Careful examination of plain films is mandatory and in cases where bone erosion or widening of the vertebral canal is evident, it is often preferable to do the myelography after having performed spinal arteriography.

Spinal Arteriography This is always an indispensable examination that provides information in the following areas [2, 4, 13, 16, 17]: diagnostic, pretherapeutic, and post-therapeutic.

Diagnosis Spinal arteriography, which was first performed by R. Djindjian in 1962, was always preceeded by global arteriography for technical reasons. It is important to note that in all cases this examination was sufficient to make the diagnosis in children [4, 5]. It is our belief that this examination should be reinstituted as a diagnostic step in young children for the following reasons: the duration of the examination, as well as the amount of irradiation have been considerably reduced; the present techniques of subtraction and the improved definition of the films permit a more precise localization with global aortography; this is possible for we have observed that these angiomas are always fed by large vessels which cannot be overlooked as may be the case with most angiomas in adults.

Precious time can therefore be saved in locating the angioma while selective catheterization should be used to identify pathological feeders. This selective means of exploration however still needs to be improved to some degree. For exploring malformations in young children up to the age of 5 years, we recommend the following procedure. Global aortography via the femoral route along with intra-arterial injection of heparin (or by retrograde catheterization via the carotid approach if under the age of 2 years). This should be accomplished by using a 3 F or 4 F catheter with manual injection, followed by selective injection, if necessary, using the same catheter which is placed at the level of the pathological feeders that have been revealed. Only cervical exploration should be selective immediately, but at this level there are only four arteries that need to be explored. It may be possible to perform global opacification of the subclavian artery, using a tourniquet placed at the proximal extremity of the arm.

Pretherapeutie Study Making the diagnosis alone is insufficient for deciding the therapeutic indication. In his thesis [3], Michel Djindjian proposed a classification of mixed and intramedullary angiomas [Fig. 1]. It should be kept in mind that this classification is based mainly on surgical observations and it has not yet been possible to make such precise observations radiologically [3, 5, 7, 12,21]. But the current radiological techniques of angiotomography and myeloangiography, and lateral view, allow this classification to be realized. The Lateral View:The value of a lateral view in the exploration cannot be overemphasized for it allows studying the intramedullary location of the arteriovenous malformation and its venous drainage, whether this be anterior or posterior, and ascending or descending. Understanding the venous drainage is an essential part of the study. Angiotomography. This is a procedure which has already been employed for detailed studies of intramedullary and meningeal arteriovenous fistulae in adults. The technique consists in studying the spinal cord laterally, starting at the depth of the anterior sulcus. By this means, the axis of the anterior spinal artery can be located as well as the length of sulcocommissural arteries and the distance between the anterior spinal artery and the AVM. Serial lateral films are then taken in order to establish the relationship between the malformation and the spinal cord.

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Using an AP view, angiotomography permits exact location of the AVM (i. e. median, retromedian, lateral), whether it is diffuse or compact, and the exact location of any associated dilatation. Myeloangiography. This associates angiography with myelography, using metrizamide. It is specially useful for evaluating the relationship between an AVM and the conus a n d / o r cauda equina. From the results of this investigation, it is possible today to define: the feeding pedicles, the size of the AVM and its location (median or lateral); its type (diffuse or compact); the existence of long or short sulcocommissural arteries; whether or not there is a close relationship between the AVM and the ASA; the existence of any intramedullary or extramedullary arterial or venous ectasia; anterior or posterior venous drainage; the location of the AMV with respect to the conus. Some difficulties in establishing the exact relationship between the spinal cord and the dilatation (i.e. IIIa, IIIb, IIIc in Fig. 1) still remain. Perhaps a solution will be found with CT. In two cases in which CT scans were made, the information obtained was insufficient, but improvements in this area should eventually provide a solution.

Postoperative Study Angiographic control is indispensable to complete any embolization or operation. First, surgical or embolization treatment may be incomplete, for the AVM may persist because of migration of the embolus. Next, there may be other vascular malformations present at the same time. Some may be extramedullary and noncommunicating, located at the same level, either metameric, epidural, vertebral or paravertebral, each presenting potential problems (compression, shunting), while others may be located at different levels. Finally, the state of normal medullary circulation is important to evaluate after therapy. Methods of Treatment

Surgery The surgical treatment of these malformations has advanced considerably over the past 18 years. The criteria for operability of intramedullary or mixed angiomas, as developed at Lariboisi6re [3] are the Following:

a localized, median, compact angioma; long sulcocommissural arteries; localized compressive dilatation with the possibility of isolated excision; characteristics of the draining veins. The surgical problem posed by extramedullary malformations is much less complicated.

Embolization This procedure also has improved over the last several years with the development of numerous stable substances: dura mater, microbeads, cyanoacrylate, releasable balloons [19]. Embolization may be the initial solution for cases of inoperable AVM, i.e. diffuse malformations. In cases where the sulcocommissural arteries are very short but very voluminous, and they empty directly into the malformation which is in direct contact with the ASA, embolization is possible. As precautions it is necessary to verify: a. that a satisfactory collateral network of the anterior spinal axis exists above and below the malformation, in case there is accidental obliteration of the anterior radicular artery supplying the AVM; b. the existence of an intermediate network (not a direct shunt) which may capture the embolus; c. that the embolus is of excellent quality. A genuine occlusion within the angioma, and not the feeding pedicles, is necessary to avoid the risk of recanalization by way of other pedicles.

Embolization and Operation Associating embolization and operation may be performed for various circumstances. Temporary preoperative occlusion of the feeding pedicle, by means of a balloon at a distance from the AVM, avoids having to perform an extensive laminectomy or indeed several at different levels. A temporary ballon makes it possible to clamp the feeding pedicle at the moment desired. Embolization of posterior or anterior and posterior pedicles before operation; Embolization of an extramedullary or vertebral AVM associated with an epidural AVM. Post surgical embolization of any residues. Embolization as an alternative to operation in cases of inoperable AVM. Clinical Results

Even though no statistical information can as yet be established, it may however be said that: the short term natural evolution of these angiomas is

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catastrophic and characterized by an unpredictable course that is marked by acute accidents; the younger the patient is and the sooner the treatment, the better are the chances for recovery. Surgical treatment opens up new hopes for improvement and even clinical and radiological cure, as will be discussed in a future article. Associating preliminary embolization or embolization and operation together at the same time in a specially equiped operating room provide new hope for the future. Embolization alone may prove effective as demonstrated in three recent cases which were embolized. Two have shown clinical improvement, and another recovered from complete non regressive paraplegia which lasted 8 weeks. His recovery which was detectable in the days following embolization, was permanent and a control arteriogram 1 year later showed complete disappearance of the angioma.

Conclusion

Spinal cord AVM in children is a grave affliction but is one of the causes of acute myelopathy which have become more and more curable, provided the following points are respected. The diagnosis must be made as early as possible during the initial onset of the symptoms; this is based on the clinical findings associated with myelography and spinal arteriography. Spinal arteriography is the key examination for making the diagnosis and should be technically of such a quality as to provide all necessary information for the therapeutic procedure required. Treatment should be performed by a radiologicalsurgical team after careful consideration of the information obtained.

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References Received: 8 September 1981 1. AminoffMJ, Logue V (1974) Clinical features of clinical vascular malformations. Brain 97: 197-210 2. Chiras J, MerlandJJ (1979) Aortic origin of the dorsospinal artery. J Neuroradiol 6:93-100 3. Djindjian M (1976) Les malformations artrrio-veineuses de la mo~lle ~pini~re et leur traitement/t propos de 150 cas. Thrse pour le Doctorat en Mrdecine, Paris VI

Dr. M.C. Rich6 Service de Neuroradiologie H6pital Lariboisirre 2 rue Ambroise Par6 Paris 10 France