Childs Nerv Syst (2008) 24:1071–1076 DOI 10.1007/s00381-008-0663-z
CASE REPORT
Conus perimedullary arteriovenous fistula in a child: unusual angio-architectural features and pathophysiology Hamilton Matushita & Jose Guilherme Caldas
Received: 18 January 2008 / Revised: 9 March 2008 / Published online: 17 June 2008 # Springer-Verlag 2008
Abstract Introduction The perimedullary arteriovenous fistulas are located on the pial surface and are usually supplied by spinal medullary arteries, that is, either by the anterior or posterior spinal arteries, with no intervening nidus between the feeder arteries and the venous drainage. The clinical findings are, more commonly, caused by progressive radiculomedullary ischemic processes secondary to steal vascular mechanism. As the vascular supply to the spinal cord and to the arteriovenous fistulas (AVF) is not shared with one another, the vascular steal phenomenon cannot be implicated in this case’s physiopathology. Most probably, the mass effect caused by the giant venous dilatation was the pathophysiological mechanism involved in this lesion Case report The authors describe the case of a 6-year-old girl with an intradural ventral arteriovenous fistula, with a giant venous dilatation, fed directly by L2 and L3 radiculomedullary arteries at the conus medullaris. There was no arterial supply to the fistula from the anterior or posterior spinal arteries. Selective spinal angiography showed an arteriovenous fistula supplied directly by two
H. Matushita (*) Division of Pediatric Neurosurgery, Department of Neurosurgery, São Paulo University Medical School, São Paulo, Brazil e-mail:
[email protected] J. G. Caldas Department of Radiology, Interventional Angiography, São Paulo University Medical School, São Paulo, Brazil H. Matushita Rua Barata Ribeiro, 237-4 andar-cjs 43/44/46, Bairro Bela Vista, São Paulo, SP Cep 01308-000, Brazil
radiculomedullary arteries, with a large draining vein caudally. Interposing the arterial and venous vessels was a giant venous aneurysmal dilatation located ventral to the conus medullaris and extending from L3 to T6. The patient was successfully treated by a surgical approach through a laminotomy from L3 to T11. Conclusion The type IV-C spinal arteriovenous malformations or perimedullary AVFs are rare lesions predominately described at the conus medullaris with various types of angio-architecture and controversial treatment. Keywords Arteriovenous malformation . Arteriovenous fistula . Conus medullaris . Spine . Children
Introduction Based on their neuroanatomy and angio-architectural features, arteriovenous lesions have been divided into arteriovenous fistulas (AVFs) and arteriovenous malformations (AVM) [4, 25]. Specifically, AVFs mean a direct shunt between the artery and vein and have been subclassified into extradural and intradural. The intradural AVFs were further divided into dorsal and ventral in relation to the spinal cord. The intradural dorsal AVFs concur with the type I spinal cord AVM or spinal dural AVFs, and the intradural ventral AVFs concur with the type IV spinal cord AVM or the perimedullary AVFs. The intradural ventral AVFs are characterized by arterial feeders from either the anterior spinal artery (ASA) or posterior spinal arteries (PSAs). We are describing a child with an intradural ventral AVF, with a giant venous dilatation, at the conus medullaris fed by left L1 and L2 radiculomedullary arteries, not connected either to the ASA or to the PSAs. Arterial supply
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Fig. 1 Antero-posterior film showing a severe thoraco-lumbar scoliosis
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contractures were present in the lower extremities. The pinprick appreciation (hypalgesia) was impaired to about T10 bilaterally and mild dysfunction of joint position sense in the lower extremities. The Babinski response was positive on both sides. She had urinary incontinence and a hypotonic anal sphincter tone with chronic constipation. Prone antero-posterior film demonstrated a severe thoracolumbar scoliosis (112°; Fig. 1). Magnetic resonance imaging of the thoracic and lumbar spine showed a large cystic mass filling the spinal canal from L3 to T6, suggesting a vascular lesion. Selective spinal angiography demonstrated high flow intradural AVF. The feeding arteries were the left first and second lumbar posterior radiculomedullary arteries. There was no contribution from either ASA or posterior spinal arteries. These feeding arteries converged to one fistulous point and enter a giant venous pouch, ventrally to the conus and spinal cord, from second lumbar to sixth thoracic vertebral level. Drainage was inferiorly by a dilated venous vein of the caudal equine vessels. The arterial supply to the shunt and the venous drainage was distinct from the blood supply to the spinal cord (Fig. 2). Discussion by multidisciplinary staff meeting led to the choice of treatment: It was decided to perform surgery
of the spinal AVF directly by the radiculomedullary arteries, with no participation of the spinal arteries, represents an unusual angio-architectural configuration of the type IV spinal AVMs. Careful evaluation of the exact angio-architecture of the spinal AVMs is extremely important in determining the most appropriate treatment. This case is very atypical considering its hemodynamic and pathophysiological characteristics.
Case report The patient is a 6-year-old girl presented with progressive toraco-lumbar deformity initially detected when she started sitting at 10 months of age. The child’s motor development was delayed; she was able to crawl, yet she had never moved her legs as well as her arms. This child developed with difficulty walking and has never controlled the sphincters. She was, initially, treated with physiotherapy and use of orthosis elsewhere but with no improvement. Within 4 years of treatment, she developed increasing motor weakness and numbness of the lower extremities. Her mother felt that the child had been an irritable girl, although she did not complain of pain. She was referred to our institution with hypothesis of spinal tumor. Her physical examination disclosed a severe thoraco-lumbar scoliosis, and she cannot stand up and walk due to a spastic paraparesis (motor strength grade I). Hyperactive stretch reflexes were present in both legs. Mild muscle atrophy and
Fig. 2 Sagittal T1-weighted MRI demonstrating a large signal void area at the thoraco-lumbar region
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Fig. 3 a. Selective injection of the first left lumbar radiculomedullary artery. a Early arterial phase—reveals the enlarged radiculomedullary artery directly feeding a giant venous aneurysm. The sudden change in caliber of the feeding artery demonstrates the point of the fistula (arrow). There is no involvement either of the ASA or the PSA. In this respect, it differs from the more common type-IV AVMs. b Later arterial phase (antero-posterior view)— shows early caudal drainage through a markedly enlarged ectatic venous system
through a posterior approach (five levels laminotomy— from L3 to T11). The main concern about endovascular treatment was the migration of the emboli to the venous side of the AVF, owing to the high flow of the fistula and the large diameter of the feeders. The surgery was carried out on June 26, 1996. A laminotomy was performed between L3 and T11. A midline dural opening disclosed two large arteries converging to a single point and supplying a direct arteriovenous shunt. The AVF was interposed by a huge aneurismal sac lied ventral to the conus and lower thoracic spinal cord, extending over seven or eight cord segments. This huge pouch had thick walls; it was tense and pulsating, pushing the spinal cord posteriorly. The rootlets of the caudal equine were pulled to the contralateral side by the aneurismal sac (Fig. 3). After clipping the two feeders that entered the distended venous pouch through a common fistulous point, the venous pouch remained tense and with little relief on the compression on the spinal cord, although the blood within Fig. 4 Selective injection of the second left lumbar radiculomedullary artery. a Early arterial phase—shows the dilated L2 (arrow) feeding the AVF. b Arterial phase—shows the same venous drainage (anteroposterior view). One major draining vein was observed to descend to its exit point at the L4–L5, foramen
it became blue as compared to the previous red color. Therefore, we decide to occlude the venous side of the fistula and empty the aneurysmal sac effectively by taping directly the sac at level T10. We did not remove the wall of the sac because it was located ventrally related to the medulla (Figs. 4 and 5). The postoperative period was uneventful. At the discharge, she neither had regained the strength or showed return of the sensation of her legs and still persisted with sphincter disturbance. Follow-up angiography demonstrated no flow and complete obliteration of the AVF. The patient experienced a gradual and progressive amelioration of neurological functions. The child has been seen in the outpatient clinics each year for 10 years. Her motor and sensory examination improved over her baseline examination during 1 year of postoperative period to a better level she had before the surgery. She walks independently but runs with great difficulties. Unfortunately, after 10 years follow-up, her
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Fig. 5 Overlapping of Fig. 3a and Fig. 4a (early arterial injections of both arteries left L1 and left L2). Arrow indicates the convergence of both arteries to the same fistulous connection
bladder functions remained unchanged, requiring intermittent bladder catheterization (Fig. 6).
Discussion Classification and angio-architecture of the spinal AVM A recent classification of spinal cord vascular lesions, proposed by Spetzler et al. [25], is based on the pathology and the angio-architecture of the lesion. Considering arteriovenous lesions, they have been divided into AVFs and AVMs. AVFs define a direct communication between the artery and a vein without a nidus or glomus of vessels at the site of transition. AVFs were further subdivided into extradural and intradural. Intradural spinal cord AVFs were finally classified into dorsal and ventral. These two latter categories are different entities in terms of anatomy, blood supplier, and physiopathology; therefore, they require distinct therapeutic approaches. The intradural dorsal AVFs were formerly classified as a “dural AVF” or “type I spinal cord AVM”. Anatomically, the fistulous connections are located at the dural sleeve covering the proximal dural root and are supplied by the dural branch of the posterior ramus of the intercostal or lumbar arteries [15, 18, 24, 25]. The most accepted mechanisms of neurological dysfunction related to spinal dorsal AVFs is venous hypertension induced by the
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retrograde flow into the perimedullary coronal venous plexus [1, 7, 12, 15, 25]. The intradural ventral AVFs were designated “the intradural perimedullary AVFs” or “type IV spinal AVMs” under the previous classifications [4, 9, 13]. The intradural ventral AVFs are characterized by the absence of a nidus and by the presence of a direct arteriovenous shunt located on the pial surface of the spinal cord. They are quite rare and have been described by Djinjian et al. [9] in 1977 and defined by Heros et al. [13] in 1986. They are fed by ASA and drain into dilated and tortuous perimedullary veins [2, 9, 13, 17, 21, 25]. Although according to the more recent classification of spinal cord AVMs [25] the nutrition of this AVF is done specifically by the ASA, other authors admit participation of the posterior spinal arteries as suppliers of the ventral AVFs [9, 10, 17, 22]. According to size and blood flow through the fistula, these lesions can be classified as IV-A, IV-B, and IV-C [3, 4, 10, 16, 20]. The ventral AVFs are located predominantly at the lower part of the spinal cord usually at the ventral surface of the conus medullaris [9, 10, 11, 14, 22]. Other spinal cord levels may be affected less frequently [6, 9, 10, 19, 22]. The likely pathophysiology accounting for the progressive myelopathy in these patients are ischemia due to shunting of the blood into the malformation [1, 2, 8, 9, 14, 25] and subarachnoid hemorrhage for those who manifest sudden neurological symptoms [11, 22]. Venous hypertension and cord ischemia caused by venous congestion and compression of the spinal cord and nerve roots by dilated vascular structures rarely results in radiculomyelopathy [11, 17, 25]. The lesion presented in this report may be classified as a giant perimedullary AVF or as a type IV-C spinal AVM, but with unusual blood suppliers, which means without
Fig. 6 Follow-up spinal angiography with no filling of the AVF (labeled arteries include: L2 dir = L2 right; L2 esq = L2 left; L3 esq = L2 left)
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involvement of the spinal arteries. Type IV-C spinal AVM, or giant AVFs are high-flow shunts with one or several large or giant feeders. Veins are severely dilated, and true venous aneurysms are encountered near the shunt. Few similar cases have been reported in the literature. Stein et al. [26] published a case of caudal equine AVF, with some similarities to our case, but supplied by branches of the internal iliac arteries not related to spinal arteries. Aydin et al. [5] described a case of perimedullary AVF fed by the left 12th radiculomedullary artery, different from the one leading to ASA. Binder et al. [8] described a 19-monthold child with a huge arterial aneurysm associated with spinal arteriovenous malformation located at the midthoracic area and supplied directly by two arteries originating from the T10th and T11th intercostal arteries on the left. Based on our findings and according to the origin of the feeders, it seems that there are two subtypes of type IV-C spinal AVM: subtype 1 includes a fistulous connection either between the anterior spinal artery or the posterior spinal arteries and perimedullary veins, and subtype 2 involves a vascular shunt directly from a branch of a radiculomedullary artery to a perimedullary veins. Understanding the exact angio-architecture of the AVF is extremely important for the choice of treatment. Currently proposed therapies include surgery alone, endovascular embolization alone, and combined forms. In general, based only on the origin of the feeder, if the lesion is fed by an anterior or posterior spinal artery (type IV-C1 spinal AVM), surgical management should be the first choice of therapy, but if the AVF is fed directly by a branch of the radiculomedullary artery (type IV-C2 spinal AVM) with no involvement of the spinal arteries, the endovascular approach is the best option. For type IV-C1 spinal AVMs, because the feeding arteries are spinal vessels, occlusion of the fistula should be carried out very precisely and close to the fistulous point. Recommended therapies of the different types of perimedullary AVFs were outlined by Barrow et al. [6]. Many factors may interfere with the recommended therapy, and the optimal treatment strategy is still controversial. The most important goal of treatment is to occlude the AVF as close as possible to the fistulous point, preserving the spinal cord circulation. Permanent deficits resulting from embolization in the ASA territory occur in up to 11% of patients [23]. Significant evolution in embolization technology in recent years may change the treatment guidelines proposed for all types of spinal cord AVMs. Physiopathological considerations The arterial feeders of our patient did not share arterial supply with the normal spinal cord, that is, neither the ASA nor the PSAs participated in the shunt. Therefore, the steal
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blood phenomenon should not be considered as a physiopathology in this case. A steal syndrome is conceivable, as the AVF is supplied by the spinal arteries. The giant venous ectasia presented in this case causing chronic spinal cord compression as the main physiopathological mechanisms involved was suggested by the mass effect revealed on the magnetic resonance imaging (MRI) and during surgery. We supposed that obliteration of the afferent vessels to the aneurysmal dilatation would not be sufficient to relieve the neural tissue from compression and chronic ischemic process. It was necessary to obliterate the efferent venous vessels to totally isolate, and finally empty, the huge venous ectasia by a direct tap and aspiration of blood. This surgical strategy probably avoided the risk of thrombosis and swelling of this venous dilatation and its consequences to the spinal cord [13, 19]. It is possible to attribute an embryonic origin of this spinal cord AVF based on chronic enlargement of the vessels and particularly of such a huge venous pouch in a very young child, as she had symptoms since infancy. We speculate that the origin of this spinal AVF is probably congenital and related to the persistence of the embryonic segmental arteries and veins at the lumbar area. The level of junction between the radicular artery and the cord may indicate the origin of the nerve root and myelomeric cord origin [23]. Regarding embryogenesis, the type IV-C spinal AVM, or arteriovenous macrofistulas as defined by Rodesch et al. [23], are considered hereditary genetic disorders developed very early during embryogenesis and usually associated with genetic hereditary diseases. Conclusion The perimedullary AVFs are a heterogeneous group of vascular anomalies related to their size, flow, and number of feeders, as well as to the type of feeders. It appears that it is important to recognize the exact arterial feeders of the fistula. The delineation of the angio-architecture of our case, compared to the literature, indicated that it might have two subtypes of type IV-C spinal AVFs: the subtype IV-C1 where the AVFs are supplied by spinal arteries and the subtype IV-C2 where the AVFs are supplied directly by radiculomedullary arteries not connected to spinal arteries. Given its blood supplier, the physiopathology involved in the present case is probably a chronic compression of the conus by the huge venous dilatation. References 1. Aminoff MJ, Barnard RO, Logue V (1974) The pathophysiology of spinal vascular malformations. J Neurol Sci 23:255–263 2. Aminoff MJ, Gutin P, Norman D (1988) Unusual type of spinal arteriovenous malformation. Neurosurgery 22:589–591
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