Spinal intradural arteriovenous fistulas acquired in late adulthood: absent spinal venous drainage in pathogenesis and pathophysiology

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1 J Neurosurg Spine 3: , 2005 Spinal intradural arteriovenous fistulas acquired in late adulthood: absent spinal venous drainage in pathogenesis and pathophysiology Report of two cases GABRIEL C. TENDER M.D., ALEXANDER O. VORTMEYER, M.D., AND EDWARD H. OLDFIELD, M.D. Surgical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland; and Department of Neurosurgery, Louisiana State University, New Orleans, Louisiana Intradural spinal arteriovenous fistulas (AVFs), a subtype of spinal arteriovenous malformation in which there is a direct communication between a spinal artery and a vein on the cord surface or in the subarachnoid space, are generally considered to be congenital lesions caused by maldevelopment of the embryonic vascular system. The authors present the cases of two patients with acquired AVFs of the terminal filum. In each patient an AVF between the distal segment of the anterior spinal artery and its accompanying vein on the terminal filum developed within 1 year of repeated lumbar myelography that had demonstrated no evidence of abnormal vascularity. In both patients spinal arteriography demonstrated the absence of medullary venous drainage in the thoracolumbar region, which, combined with the arterialized venous input from the AVF, permitted the development of venous congestion and myelopathy. The involved segment of the terminal filum was excised; in vitro microarteriography and the histopathological examination demonstrated a single, simple arteriovenous connection in both patients. The findings in these cases indicate that intradural AVF can spontaneously arise in later life. The development of these lesions and/or their clinical manifestation may require not only the presence of the AVF, but also deficiency of medullary spinal venous drainage. The epidemiology and anatomy of intradural AVFs are compatible with an acquired origin in many cases. KEY WORDS arteriovenous fistula arteriovenous malformation terminal filum lumbar puncture myelopathy venous congestion W ITH the recognition of spinal dural AVFs in the late 1970s and early 1980s, 18,19 perimedullary AVFs in 1977, 9 the clinical importance of cavernous angiomas, and an increased understanding of the pathophysiology underlying the natural history and clinical presentation of the various types of spinal AVMs, it has become clear that each of these major types is a distinct biological entity. 23 This in turn requires classification of spinal AVMs to establish terminology that accurately describes the lesion and, thus, provides a logical categorization based on biologically distinct categories rather than on the use of older terms and classification schemes 1) that were based on mistaken understanding of the true Abbreviations used in this paper: AVF = arteriovenous fistula; AVM = arteriovenous malformation; ASA = anterior spinal artery; MR = magnetic resonance. nature of the lesions; 2) that used abstract terms, such as Type I spinal AVM, rather than easily understood and clearly descriptive terms to describe the various lesions; and 3) that, because they were abstract terms, led to substantially different usage of the same term by different authors. 3,7 Four types of spinal vascular malformations with distinctive biological features (anatomy, pathogenesis, pathophysiology, epidemiology, and clinical features) are now recognized: dural AVFs, intradural vascular malformations (AVMs of the spinal cord and intradural AVFs, also known as perimedullary AVFs), and cavernous angiomas of the spinal cord (Table 1). 23 In dural AVFs the nidus of the lesion is embedded in the dura mater, usually in the spinal nerve root sleeve and the contiguous dura. In the intradural lesions the arteriovenous shunt is either buried in the substance of the spinal cord (spinal cord AVMs) or is in the pia mater or subarachnoid space (perimedullary AVFs). The origin and pathophysiology of the spinal peri- 488 J. Neurosurg: Spine / Volume 3 / December, 2005

2 Adult-onset spinal arteriovenous fistula TABLE 1 Classification of spinal vascular abnormalities based on biological features* A) dural AVFs B) intradural AVMs 1) spinal cord AVMs a) juvenile AVMs b) glomus AVMs 2) AVF (perimedullary AVFs) C) cavernous angiomas * Adapted from Oldfield and colleagues, medullary AVFs are incompletely elucidated. Their origin is generally believed to be congenital. We present two cases in which the findings indicate that an intradural AVF can be acquired without a precipitating event. Thus, many intradural AVFs may be acquired and are associated with deficiency of medullary venous drainage of the spinal cord, as is the circumstance with spinal dural AVFs. Case Reports Case 1 History. This 70-year-old African-American man presented with a 7-year history of low-back pain and progressive bilateral lower-extremity weakness. In 1982, 18 months before admission, spinal computerized tomography scanning and repeated lumbar myelography revealed lumbar stenosis but no evidence of abnormal vessels. He underwent an L-4, L-5, and partial L-3 decompressive laminectomy for spinal stenosis, and his symptoms were relieved. One year later he was hospitalized with worsening bilateral leg weakness, urinary retention, and constipation. Lumbar myelography then demonstrated T11 L3 serpentine filling defects consistent with the presence of an AVM, which had not been documented on any of the previous myelographic studies. The patient was referred to the National Institutes of Health for assessment. Examination. Neurological examination revealed symmetrical Grade 3/5 lower-extremity motor weakness and decreased rectal tone. There was diminished light touch and pinprick sensation in both legs, especially below the knees. The patient could not stand or walk because of leg weakness. Lumbar myelography revealed serpentine filling defects at the thoracolumbar junction (Fig. 1A). After selective injection of the left 11th thoracic intercostal artery spinal arteriography demonstrated that the artery of Adamkiewicz filled a dilated ASA, the distal segment of which extended to the L-4 level where it emptied immediately into an early filling vein; flow then continued upward to fill a dilated, tortuous venous system on the spinal cord surface, extending rostrally to the cranial venous system. The precise site of the artery vein transition was visible as an abrupt expansion of the vessel size (Fig. 1B, white arrows). Operation. After an L-3 laminectomy and opening of the dura mater over the region of the previous and current laminectomy, we observed the dilated, tortuous intrathecal venous system carrying reddish, arterialized blood. An AVF was identified in the pia mater of the terminal filum at L-4 (Fig. 1C). The arachnoid in this region was thick and adherent to the nerve roots of the cauda equina. The segment of the terminal filum containing the junction between the feeding artery and draining vein was removed. After cannulating the distal ASA, serial in vitro arteriographic examination of the pathological specimen (Fig. 1D) demonstrated the distal segment of the feeding artery, the arteriovenous junction, the dilated draining vein, and a small, undilated distal extension of the ASA supplying the terminal filum below the level of the AVF. Postoperative Course. The patient s neurological function improved progressively during the next several weeks. At 6 weeks after surgery spinal arteriography revealed that the size of the ASA had returned to normal; no AVF or abnormal flow into an early draining vein was documented. He was able to walk with a cane 1 year after the operation. Case 2 History. This 58-year-old Caucasian man had an 18- year history of bilateral leg weakness and paresthesias. He underwent lumbar laminectomy for spinal stenosis on three occasions (and was evaluated with myelography at least once before each procedure), experiencing partial improvement after the first two operations but worsening symptoms after the third. In 1991, 1 year before admission, he became wheelchair bound and urinary retention and constipation developed. Lumbar MR imaging demonstrated flow voids consistent with the presence of a vascular malformation. He was referred to the National Institutes of Health for assessment. Examination. Neurological examination revealed bilateral lower-extremity weakness, mostly in the hip flexors and foot extensors. There was decreased pinprick, light touch, and vibratory sensation below the T-10 dermatome. The lower extremities were hyperreflexive. He could not stand or walk because of motor weakness. Lumbar MR imaging demonstrated flow voids in the T11 L3 region, a dilated coronal venous plexus extending from the thoracic to the cervical spine and the posterior fossa, and a hyperintense signal in the thoracic segments of the spinal cord on T 2 -weighted images (Fig. 2A). Selective spinal arteriography demonstrated an intradural AVF at the upper L-2 vertebral level, supplied by the distal segment of an enlarged ASA, which itself was fed by the artery of Adamkiewicz from the left ninth thoracic intercostal injection (Fig. 2B and C). Venous drainage extended rostrally toward the cranial venous system without lateral venous drainage (Fig. 2B and C). Operation. An L1 2 laminectomy exposed the thick, opaque and adherent dura mater overlying the fistula. Intraoperative Doppler ultrasonography was performed to evaluate the content of the spinal canal (Fig. 2D). Following dissection of the thick and adherent arachnoid feeding artery draining vein, the junction was identified at the site of the AVF on the terminal filum (Fig. 2E). Very high pressure in the draining vein was evident when it was punctured with a 25-gauge needle (Fig. 2F). After en bloc removal of the AVF and the terminal filum in the involved region, in vitro arteriographic examination of the surgical J. Neurosurg: Spine / Volume 3 / December,

3 G. C. Tender, A. O. Vortmeyer, and E. H. Oldfield FIG. 1. Case 1. A: Lumbar myelogram demonstrating persistent lumbar stenosis and serpentine filling defects suggestive of a vascular malformation. The engorged, tortuous subarachnoid vessels were not seen on previously obtained myelograms, even the most recent study 1 year previously. B: Arterial (left two images) and venous (right two images) phases of selective spinal angiography demonstrating the AVF (white arrows) at the L4 5 interspace supplied by a dilated ASA. The small arrows indicate the direction of flow. The large arrows indicate the region of the AVF demonstrated in C and D. Note the rostral venous drainage of the AVF toward the cranial venous system and the absence of lateral venous drainage into the epidural veins. C: Intraoperative photographs demonstrating the expanded distal portion of the terminal filum, the distal extension of the ASA (yellow arrows), and the veins draining the AVF. D: In vitro arteriograms of the surgical specimen (arterial injection) demonstrating the distal part of the feeding artery, the dilated proximal draining vein, the site of the artery vein transition (white arrow), and a small arterial branch supplying the terminal filum below the AVF (right-pointing arrowhead in image on the far right). The left-pointing arrowheads show the same level of the loop in the distal ASA and relate this level in B and C. Note the abrupt transition between the artery and vein (white arrows in B, C, and D). specimen was performed via cannulation and injection of the vein draining the AVF (Fig. 2G). Postoperative spinal arteriography demonstrated resolution of the AVF and normalization of the size of the ASA (Fig. 2B [right]). Histological evaluation of the specimen showed vascular structures with venous and arterial-type vessel walls. An abrupt transition occurred between a venous vessel and an arterial vessel with degeneration of the internal elastic lamina and atheromatous changes (Fig. 2H). Postoperative Course. Sensation and motor function improved significantly in the 1st weeks after surgery. The patient walked with a cane at 1 year postoperatively. Discussion In our two cases acquired terminal filum AVFs were associated with cranial venous drainage and progressive myelopathy due to venous hypertension; the findings in these cases raise several questions. Why would an intradural lumbar region AVF drain its blood rostrally all the way to the cranial venous system instead of laterally into the epidural venous system? Is the late-onset adult development of pial AVFs in these patients related to excess venous pressure caused by the deficiency of normal pathways for spinal venous drainage? Or vice versa, might the deficiency of spinal medullary venous drainage be caused by progressive occlusion of medullary veins by the high flow and pressure imposed on them by the presence of the AVF? Does the formation of an intradural spinal AVF caused by venous hypertension require deficient spinal venous drainage? Intradural Spinal AVFs A direct communication between an enlarged spinal artery and vein, usually between the ASA and the coronal venous plexus, distinguishes the perimedullary AVFs, which compose approximately 10 to 20% of all spinal AVMs. 1,14,16 The fistulous communication is almost always in the pia mater on the surface of the spinal cord. The anatomical distribution of the fistula along the long axis of the spine is bimodal (Fig. 3), predominantly in the thoracolumbar region, particularly at the conus medullaris and, to a lesser extent, in the upper cervical region. Males and females are equally affected. For therapeutic purposes, Merland, et al., 21 categorized perimedullary AVFs into three distinct types. Type I is a small, simple fistula supplied by a single feeding artery, usually the terminal portion of a thin ASA, but in some instances by a posterior spinal artery. The flow through the fistula is usually slow and ascending in the vessels of the coronal venous plexus, which are only slightly tortuous and dilated. Type II AVFs are supplied by one or two main feeding arteries via several distinct arterial pedicles that 490 J. Neurosurg: Spine / Volume 3 / December, 2005

4 Adult-onset spinal arteriovenous fistula FIG. 2. Case 2. A: Sagittal T 2 -weighted MR images of the thoracic (left) and lumbar (center) spine, revealing flow voids in the subarachnoid space indicative of a vascular lesion. The high signal in the spinal cord from the midthoracic level to the conus medullaris is consistent with changes in the cord due to venous hypertension. The sagittal T 1 -weighted contrast-enhanced cervical image (right) demonstrates dilated perimedullary veins of the coronal venous plexus draining the excess blood from the AVF at L1 2 all the way to the cranial venous system. B: Anteroposterior (left and right images) and lateral (center inset) arteriograms obtained after selective injection of the ninth left thoracic intercostal artery, revealing the AVF (white arrows) supplied by an enlarged and tortuous ASA. There is an abrupt transition between the feeding artery and draining vein (white arrows). Residual contrast material from previous myelographic examinations is seen in the lumbar thecal sac (center inset). The right-sided arteriogram was acquired 6 weeks after surgery. The horizontal black arrows indicate an outline of the conus medullaris by surface vessels. The small black arrows in the inset demonstrate the direction of blood flow. The images are positioned at the same level. Note a reduction in size of the ASA and the absence of filling caudal to the conus medullaris after excision of the AVF (right image). C: Lateral view of digital subtraction arteriogram demonstrating sequential filling of the AVF (white arrows) from the arterial (anterior) through the early venous (posterior) phases. Note the abrupt transition from artery to vein at AVF (white arrows). The small black arrows indicate the direction of blood flow. D: Sagittal view of the intraoperative Doppler ultrasonography study with the probe placed on the posterior dural sac (yellow arrow). The distal ASA flowing caudally is shown in red and the venous drainage rostrally is shown in blue. The AVF is at the transition from caudal to rostral flow (white arrow). E and F: Intraoperative photographs demonstrating the proximal portion of the vein draining the AVF before (E) and after (F) puncturing with a 25-gauge needle. The AVF is at level of white arrow in E. Note the pulsatile jet of bleeding produced by puncturing the vein draining the AVF (F). G: In vitro arteriogram of the surgical specimen obtained after retrograde injection of the draining vein, revealing the dilated draining vein, the feeding artery, and the site of the AVF between the two vessels (arrow). (C, D, and G are sagittal images with anterior position on left.) H: Photomicrograph of the AVF; note the abrupt transition from arterial-type (A) to venous-type (V) vessel (arrow). Elastica van Gieson stain. J. Neurosurg: Spine / Volume 3 / December,

5 G. C. Tender, A. O. Vortmeyer, and E. H. Oldfield FIG. 3. Graphs showing the distribution of cases involving perimedullary AVFs stratified by gender, age at diagnosis, and level of AVF along the long axis of the spine. Adapted from Oldfield, et al., converge to multiple discrete shunts and drain into a dilated and tortuous venous system with a relatively high flow rate. Type III AVFs, composing the majority of the perimedullary AVFs, are single giant AVFs with very high blood flow located in the cervical or lower thoracolumbar levels. They are fed by several branches of the posterior or anterior spinal arteries, which are hugely dilated and which converge into a single shunt draining into a giant venous ectasia. 14,22 Initially it appeared as though there were no distinctive features of clinical manifestation among the various types of perimedullary AVFs, but as more experience has been gained it has become apparent that only the Types II and III AVFs hemorrhage or compress the spinal cord by venous ectasia. 22 Most patients, regardless of which type of lesion they harbor, present with myelopathy but no hemorrhage (80%), 28 and paraplegia gradually progresses within 5 to 7 years of symptom onset. 4,14,22,28 As in the patient in our Case 2, MR imaging findings include flow voids reflecting engorged veins on the cord surface and T 2 -weighted hyperintensity of the spinal cord reflecting venous congestion. 2,11 Thus, most patients experience gradually progressive neurological loss 22,28 that is similar to the course associated with the venous hypertension known to underlie the myelopathy in patients with spinal dural AVFs. The existence of perimedullary AVFs in early childhood suggests a developmental origin in some patients; however, most patients present as adults (Fig. 3). Limited Venous Drainage Venous drainage of the normal spinal cord initially occurs via sulcal veins in the anterior median fissure and radial veins in the posterior and anterolateral portions of the spinal cord, which drain into the coronal venous plexus on the cord surface. 12 This pial venous plexus is drained by medullary veins to the epidural venous plexus. Eight to 12 medullary veins, present sporadically along the long axis of the spinal cord, cross the subarachnoid space and penetrate the dura adjacent to the dural penetration of the nerve roots, carrying the venous blood into the epidural vertebral venous (Batson) system. 12 As in the cranial venous system, the veins within the intrathecal spinal space lack valves. 12,29 In the region of the cervicomedullary junction the venous system of the brainstem and the spinal cord freely communicate. In 1970, shortly after the introduction of selective spinal arteriography, Di Chiro and Doppman 8 and Djindjian, et al., 10 noted the peculiar distribution of the venous drainage of certain spinal AVMs in the lower half of the spinal column, extending all the way to the cranial venous system. Observation of cranial venous drainage of the intradural spinal AVFs began in 1986 when Heros and colleagues 16 described dilated and engorged veins in the posterior fossa in a patient with a midthoracic pial AVF. Additional patients with lower thoracic or lumbar intradural spinal AVFs and cranial venous drainage have also been described. 4,31 Barrow, et al., 4 directly quantified venous hypertension in the venous drainage of two patients with intradural spinal AVFs and progressive myelopathy; they related the venous pressures to the clinical findings. This mechanism must account for myelopathy in cases of the Type I intradural spinal AVFs, because they do not hemorrhage, are not associated with venous ectasia and cord compression, and their rate of transit from the arterial to the venous system is much too slow to produce vascular steal. In both of our patients there was extensive rostral venous drainage from an AVF in the terminal filum to the posterior fossa in the absence of lateral venous drainage to the epidural venous system. Thus, the pathogenesis of the 492 J. Neurosurg: Spine / Volume 3 / December, 2005

6 Adult-onset spinal arteriovenous fistula venous hypertension and cranial venous drainage in cases of intradural spinal AVFs is not only a result of the AVF but is combined with the deficiency of functional medullary veins, the veins that would normally carry the blood from the spinal cord into the epidural venous system. Common Features of Perimedullary AVFs and Spinal Dural AVFs Dural AVFs, the most common form of spinal AVMs, 13,25 are located in the dura mater of a nerve root sleeve and the adjacent spinal dura. 18,20,24 These lesions occur predominantly in older men and are concentrated in the thoracolumbar region. 25,29 The feeding artery is a dural branch of an intervertebral artery. 20,24 Patients present with slowly progressive myelopathy produced by venous congestion of the spinal cord. 24,28,30 The following factors suggest that dural AVFs are acquired lesions: the onset of symptoms in the latter half of adulthood, the strong predilection for the lower spine, the absence of medullary veins, the predominant occurrence in men, and the capacity to develop similar lesions by mechanisms that are known to be acquired (such as traumatic paraspinal AVFs 32 and postoperative dural AVFs 33 ). The pathophysiology of the progressive myelopathy associated with them is venous hypertension. 15,24 The absence 19,21,24,28 of normal paths of venous drainage associated with spinal dural AVFs was first noted by Logue, 19 who asked Why are the abnormal veins on the back of the spinal cord distended over such a long length when there are normally eight to twelve large anterior medullary veins arranged at fairly close intervals along the cord, all potentially capable of draining excess blood into the extradural venous plexus and so reducing the high venous pressure? Within a few years these observations had also been made and emphasized by others. 21,24,28 The limited venous drainage is probably a requirement for the development of venous hypertension and thus for the clinical manifestation of the spinal dural AVFs as the absence of normal spinal venous drainage consistently accompanies them. In our two cases of intradural AVFs the excess blood flow through the AVF combined with the absence, or loss, of medullary veins the veins that normally drain blood from the coronal venous plexus on the spinal cord surface to the epidural venous system led to venous hypertension with dilation and tortuosity of the coronal venous plexus rostrally all the way to the cranial venous system. Evidence of venous congestion included the abnormal cord signal on T 2 -weighted MR images and the observation that when the draining vein was punctured it was under arterial pressure. Because the spinal intrathecal venous system has no valves to prevent retrograde flow, this high pressure is transmitted to the spinal cord, leading to decreased spinal perfusion pressure, cord engorgement, and myelopathy. If our patients had normal pathways for venous drainage from the spinal cord, venous congestion of the cord may not have developed and the presence of the fistula may have remained clinically silent. The circumstances observed in our cases an acquired AVF in late adulthood, a simple AVF, and venous congestion associated with deficient medullary venous drainage are similar to the features in cases of spinal dural AVFs; the only obvious difference is the precise anatomical site of the AVF. Possibility of Lumbar Puncture Causing Intradural AVFs In both of our patients an AVF between the distal segment of the ASA and its accompanying vein on the terminal filum developed within 1 year of repeated lumbar myelography that revealed no evidence of abnormal vascularity. Myelography is a sensitive diagnostic procedure with which to detect the presence of a dilated, tortuous coronal venous plexus associated with arteriovenous shunting. 23 Thus, it is unlikely that the AVF was present at the time the series of myelograms was obtained. Another possibility for the origin of the perimedullary AVF in these patients is that in each case one of the several prior lumbar punctures created an intradural arteriovenous communication in the terminal filum. Symptomatic spinal stenosis, which, when evaluated with myelography often requires multiple needle punctures for successful myelography, may increase the risk of traumatic vascular injury and AVF formation by lumbar puncture. Many AVFs in the central nervous system and at extra central nervous system sites have been produced by puncture wounds and by missile injuries. 27 Cerebral arteriography after percutaneous arterial puncture during femoral, 26 carotid, or vertebral arteriography is associated with the risk of AVF formation, 5,6 and needle biopsy procedures of the kidney 17 or liver occasionally produce low-flow AVFs. In both our patients spinal stenosis was present, and each underwent repeated myelographic examinations to document the source of his recurrent symptoms. Simultaneous puncture of the distal ASA and its accompanying vein on the terminal filum may have led to AVF formation. The AVFs were in the region of the spinal axis susceptible to injury by lumbar puncture. Moreover, the myelographic (Cases 1 and 2) and MR imaging (Case 2) studies were interpreted as normal 1 year before the presence of obvious abnormal vessels was demonstrated by these modalities when the fistulas were discovered. Even if lumbar puncture caused the AVF, rather than its forming spontaneously, a deficiency of medullary venous drainage accompanied the clinical manifestation of the AVF; this again suggests that limited regional venous drainage from the coronal plexus to the epidural venous plexus may be a necessary associated feature for venous congestion, venous hypertension, and myelopathy to develop in patients with spinal AVFs, whether the lesion is acquired iatrogenically or otherwise. Another possibility is that the effects of decompressive laminectomy limited the regional venous drainage from the spinal cord into the epidural venous system. This seems unlikely, however, because even if local surgery altered the medullary venous drainage in the lumbar region, it would have no effect on the remaining medullary veins in the thoracic and cervical regions, regions that normally contain most of the medullary veins. 12 Conclusions These aforementioned observations suggest that many perimedullary AVFs, which mainly manifest in adults, may have a pathogenesis that is acquired, and are not congenital as had previously been assumed, and indicate that their associated pathophysiological features (venous congestion, venous hypertension, and myelopathy) are not J. Neurosurg: Spine / Volume 3 / December,

7 G. C. Tender, A. O. Vortmeyer, and E. H. Oldfield only related to the AVF but are also linked to a deficiency in spinal medullary venous drainage. Thus, with the exception of the site of the AVF, most of their features resemble those of spinal dural AVFs. Many of these lesions may be acquired, and their pathogenesis may be related to absent medullary venous drainage pathways. Whether the efficiency of medullary veins associated with spinal dural or perimedullary AVFs, as noted here, is present from birth or is acquired later in life, perhaps as a result of the high flow and pressure in the medullary veins, is unknown. References 1. Aminoff MJ, Gutin PH, Norman D: Unusual type of spinal arteriovenous malformation. Neurosurgery 22: , Andersson T, van Dijk JM, Willinsky RA: Venous manifestations of spinal arteriovenous fistulas. Neuroimaging Clin N Am 13:73 93, Baker HL, Love JG, Layton DD Jr: Angiographic and surgical aspects of spinal cord vascular anomalies. 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Oldfield, M.D., Surgical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 10 Center Drive, Building 10, Room 5D37, Bethesda, Maryland eo10d@ nih.gov. 494 J. Neurosurg: Spine / Volume 3 / December, 2005