Vascular: Hemorrhage Intraventricular Hemorrhage as a False Localizing Sign of a Thoracolumbar Arteriovenous Malformation: Case Report Pál Barzó, M.D., Ph.D.,* Erika Vörös, M.D.,† and Mihály Bodosi, M.D., Ph.D.* Departments of Neurosurgery and †Radiology, Albert Szent-Györgyi Medical University, Szeged, Hungary Barzó P, Vörös E, Bodosi M. Intraventricular hemorrhage as a false localizing sign of a thoracolumbar arteriovenous malformation: case report. Surg Neurol 1999;51:430 – 4. BACKGROUND Spinal arteriovenous malformation (SAVM) is a relatively rare disease characterized by a high incidence of intramedullary and subarachnoid haemorrhage. When the hemorrhage is profuse and the SAVM is in the cervical region the symptoms (disturbance of consiousness, papilledema, cranial nerve palsies, and convulsions) may be so severe and rapid in their onset that they may be mistaken for intracranial hemorrhage. We report here on a patient with a SAVM at T10 –12, which bled intracranially, mainly intraventricularly, and resulted first in respiratory arrest and unconsciousness. CASE DESCRIPTION The patient had been well until he was 28 years old when, during intercourse, he suffered a terrible headache and suddenly lost consciousness, with a transient respiratory arrest. He was also noted to have right hemiparesis. A computed tomography scan demonstrated intraventricular hemorrhage. After a 24-hour period of artificial ventilation the patient regained consciousness and the right arm paresis completely recovered, but a gradual worsening of the motor function of the left leg developed. Digital subtraction angiography did not demonstrate any intracranial source of bleeding, whereas spinal angiography revealed a SAVM located at the medullary cone, which was totally removed by surgery. CONCLUSION The case reported here raises several important issues. First, the advisability of spinal magnetic resonance imaging in the investigation of intraventricular (and subarachnoid) hemorrhage in patients with no demonstrable intracranial source. Secondly, the benefits of early diagnosis and reestablishment of the spinal cord circulation before the onset of thrombosis and the progressive phase of myelopathy. Finally, the necessity of complete Address reprint requests to: Dr. Pál Barzó, Department of Neurosurgery, Albert Szent-Györgyi Medical University, Semmelweis u. 6 sz., Szeged, Hungary. Received April 11, 1997; accepted October 28, 1997. 0090-3019/99/$–see front matter PII S0090-3019(98)00044-5 obliteration and treatment of SAVMs even in patients with fixed neurologic deficits, because rebleeding of lower thoracic or lumbar SAVMs can lead to impairment at a higher level with severe or lethal consequences. © 1999 by Elsevier Science Inc. KEY WORDS Thoracolumbar AVM, intraventricular hemorrhage, respiratory arrest, unconsciousness. pinal arteriovenous malformation (SAVM) is a relatively rare disease characterized by a high incidence of hemorrhage. It has been reported that intramedullary and subarachnoid hemorrhage (hematomyelia) are the most striking clinical findings; they occur in over 50% of the patients, and result in spinal cord damage, arachnoiditis, scarring, and secondary ischemia to the spinal cord [6,14,15]. Patients with medullary SAVMs may present several other signs and symptoms, such as progressive chronic radiculomyelopathy (Foix-Alajouanine), root symptoms, spinal cord compression, ischemia, venous thrombosis, and infarction [4]. Furthermore, when the hemorrhage is profuse and the SAVM is in the cervical region, there may be a disturbance of consciousness, papilledema, cranial nerve palsies, and convulsions. These symptoms may be so severe and rapid in their onset that they may be mistaken for intracranial hemorrhage. As the following case demonstrates, even patients with lower medullary SAVMs may display the typical syndrome of subarachnoid and intraventricular hemorrhage. We report here on a patient with a SAVM at T10 –12 that bled intracranially, mainly intraventricularly, and resulted first in respiratory arrest and unconsciousness. S © 1999 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010 Intraventricular Blood as a False Sign Surg Neurol 431 1999;51:430 –4 ventral and the dorsal surfaces of the spinal cord and partially by vessels descending on the dorsal surface (Figure 2a,b). On magnetic resonance (MR) examination, the heterogenity of the local magnetic field indicated a nonhomogenous mass at the level of T11–12; this comprised a mixed mass of SAVM, hemorrhage, and edema. Part of the SAVM and some of the large perimedullary vessels, the radiculomedullary artery and the draining veins, both of which showed signal loss, were identified on T1and T2-weighted images (Figure 3). MR T2 images of the craniocervical region indicated a large median aperture (foramen Magendi) of the fourth ventricle. 1 Axial CT image without contrast enhancement, showing hemorrhage in the occipital horns. Case Report The patient, a young economist, had been well until he was 28 years old when, during intercourse, he suffered a terrible headache and suddenly lost consciousness, with a transient respiratory arrest. He was also noted to have right hemiparesis and was taken to the local hospital. Over the following 24 hours, his respiration normalized under assisted ventilation, he regained consciousness, and the motor function in the right arm was restored. A computed tomography (CT) scan demonstrated intraventricular hemorrhage (Figure 1). Cerebral angiography did not reveal any source of bleeding. During the next 7 days, the rectal sphincter tone diminished, urinary retention developed, requiring placement of an indwelling catheter, and the patient gradually lost all the lower extremity function on the left and became paraplegic, with a total loss of sensation below T-12. At the time of his admission to our institution, 2 weeks after the attack, the neurologic examination revealed flaccid paraplegia, complete sensory loss below T-12, and urinary incontinence. As repeated angiography of the cranial vessels did not show any source of bleeding, spinal arteriography was performed. Selective injection of the right T-9 intercostal artery (Adamkiewicz artery) and the right L-3 iliolumbar, radiculopial artery revealed a SAVM at T10 –12 (Figure 2a,b). The SAVM was drained mainly by serpentine vessels ascending on both the OPERATION The patient underwent surgery 18 days after his attack. A laminectomy was performed at T10 –11 level. The dura was expanded and dark blue. Widespread subarachnoid hemorrhage and grossly abnormal vascular convolutions were seen over the right posterolateral aspects of the conus medullaris. The arachnoid was opened on the right side, exposing the intradural and extramedullar components of the SAVM. A large arterial feeder to the SAVM, previously visualized by angiography, was identified as the radiculopial artery. After occlusion of this artery, the nidus was mobilized medially and dorsally (it was partially demarcated by the hemorrhage), exposing the main draining vein, which was totally thrombosed. On the right side, most of the nerve roots were damaged by the hemorrhage. After the other large and multiple small feeders extending between the left nerve roots and the SAVM had been coagulated, the nidus and the thrombosed vein were removed completely. POSTOPERATIVE COURSE In the 4 weeks after the procedure, no improvement was observed in the lower extremity function, the bowel function or the bladder function. Discussion As far as we are aware, this is the first case report demonstrating that intraventricular and subarachnoid hemorrhage secondary to a ruptured lower SAVM can present with symptoms of unconsciousness and respiratory arrest. Although the diagnosis of lower spinal SAVM is assisted by maintaining a high level of alertness for signs of spinal cord symptoms, several important findings in our patient suggested intracranial hemorrhage and no symptoms of the spinal cord lesion were initially observed. The absence of an intracranial source of hemorrhage, as assessed by digital subtraction cerebral 432 Surg Neurol 1999;51:430 –4 Barzó et al Selective angiography in the right T-9 intercostal artery confirmed the SAVM fed by a radiculomedullar (Adamkiewicz) artery (a; arrowhead). The main feeder of the SAVM is presented by a radiculopial artery originating from the L-3 iliolumbar artery (b; arrowheads). The SAVM was drained mainly by serpentine vessels ascending on both the ventral and the dorsal surfaces of the spinal cord and partially by vessels descending on the dorsal surface. 2 angiography, and the signs of a spinal cord lesion on the day of admission led us to suspect SAVM, and the angiography was continued in the same session at the craniocervical, cervical and thoracolumbar levels. Angiography of the Adamkiewicz (T-9) and L-3 iliolumbar arteries demonstrated an extramedullary SAVM at the T11-L1 level posterior to the medullary cone. Unfortunately, the time interval between the onset and the definitive diagnosis and surgery was too long. This leads us to conclude that in cases where the intracranial source of hemorrhage remains unknown, spinal MR imaging should be performed to exclude or reveal a spinal lesion as soon as possible. This is supported by two other reported cases of subarachnoid hemorrhage and concurrent intracranial and spinal cord AVMs. In both cases, the clinical and radiographic criteria and the surgical findings suggested that the latter was the source of the hemorrhage [9,12]. The outcome of the present patient, however, indicates another important conclusion. The patient recovered completely from the right hemiparesis before the rapid and progressive loss of neurologic functions in the lower extremity developed. We explain this late deficit in terms of gradually progressive venous thrombosis because of the venous congestion after the apoplectic event. This is supported by the intraoperative finding of venous thrombosis. The symptoms were very similar to those described first by Foix and Alajouanine and by others [5,7,10,13] in subacute progressive myelopathy because of partial or complete thrombosis of a SAVM. Although typical clinical findings of progressive paraplegia, sensory changes, and loss of sphincter control are uniformly present and the diagnosis of subacute myelopathy has only been considered when clinical changes occur in a patient with vascular malformation in the absence of hemorrhage, it is suggested that in our case the venous congestion and thrombosis resulted from the reduced outflow because of the local effect of the hemorrhage. Our patient underwent surgery with symptoms of spinal cord transection and no clinical improvement was observed. This may indicate that the mechanical effect played only a secondary role in the cord damage. The observation is important clinically in that the early diagnosis and proper Intraventricular Blood as a False Sign The midsagittal T1-weighted image shows part of the nidus at the dorsal level of T-11 (white arrowhead). High-signal intensity around the medullar cone and the nerve roots correspond to subacute subarachnoid hemorrmage (black arrowheads). 3 management of SAVM and venous congestion are likely to result in a more successful outcome. Only a few previous reports have focused on the rebleeding risk of SAVMs. Aminoff and Louge analyzed the largest number of patients, but even their group of 53 patients was too small to permit an accurate assessment of the risk [1,2]. Of those 53 patients, 3 died within a few days of the initial bleeding, 4 were operated on, and 5 were lost to further analysis. Among the remaining 41 patients, 22 (54%) had a second subarachnoid hemorrhage and 4 of these 22 (18%, or 9% of the 41) died. Second hemorrhages occurred as early as within 24 hours after the first episode to well over 5 years subsequently. In other series, investigation of the incidence of hemorrhage of cervical SAVMs revealed an even less favorable prognosis: 78% [4], 58% [15], and 57% [6]. However, most of the deaths from intracranial hemorrhage secondary to SAVMs were attributable to SAH, hematomyelia, and complications of neurologic deficits (septicemia, decubitus, Surg Neurol 433 1999;51:430 –4 or urinary tract infection), and it is necessary to take into account the direct (high cord, brain stem, and hypothalamic) effects of the hemorrhage, such as headache, unconsciousness, convulsion, cranial nerve palsies, and respiratory muscle paralysis [3,4,8,11]. On the basis of these observations and on our findings relating to the present case, in a patient with a permanent deficit or clinical cord transection it is unlikely that treatment will be of functional benefit, but treatment is nonetheless indicated, as repeated life-threatening spinal hemorrhage can be avoided only by proper closure or resection of the malformation. When all these observations are considered in concert, the case reported here raises several important issues. First, we would again like to stress the advisability of spinal MR imaging in the investigation of subarachnoid (and intraventricular) hemorrhage in patients with no demonstrable intracranial source. Second, early diagnosis and reestablishment of the spinal cord circulation should be pursued aggressively before the onset of thrombosis and the rapidly progressive phase of myelopathy. This is especially important when the initial symptoms are followed by rapid deterioration. Finally, we strongly suggest complete obliteration and treatment of SAVMs even in patients with permanent neurologic deficits, because rebleeding of lower thoracic or lumbar AVMs can also be life threatening. REFERENCES 1. Aminoff MJ. Spinal angiomas. Oxford: Blackwell, 1976. 2. Aminoff MJ, Logue V. The prognosis of patients with spinal vascular malformations. Brain 1974;97:197– 210. 3. Berenstein A, Choi IS, Neophitydes A, Benjamin V. Endovascular treatment of spinal cord arteriovenous malformations (SCAVMs). 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J Neurosurg 1987;67:795– 802. 15. Yaşargil MG, Symon L, Teddy PG. Arteriovenous malformations of the spinal cord. In: Symon L, ed. Advances and technical standards in neurosurgery. Vol 11. Wien: Springer, 1984:61–102. COMMENTARY This is an interesting case of severe intraventricular hemorrhage associated with a low thoracic spinal cord AVM. The diagnosis was made by MRI and supported by spinal angiography. The venous thrombosis of the AVM proven at surgery is probably responsible for the secondary deterioration of the patient. However, it is through a different mechanism than the Foix and Alajouanine syndrome, which is a progressive necrotizing myelitis second- Barzó et al ary to spinal cord venous hypertension associated with a dural fistula. Gerard Debrun, M.D. Departments of Neurosurgery and Radiology University of Illinois at Chicago Chicago, Illinois The question of SAH and coma from a spinal arteriovenous malformation is of interest. It is a rare phenomenon, and ordinarily is preceded by neck or back pain at the moment of onset. Although most have been associated with cervical or dorsal malformations, in a series published in 1982 [1], one such case was attributable to a conus malformation. Finally, considering the frequency of SAH patients whose angiograms are negative at least initially or even on repeat 2 or 3 weeks later, and the extreme rarity of this presentation as an indication of a spinal AVM, I would certainly not be willing to recommend spinal study during the brief window of opportunity before spinal symptoms might occur. Leonard I. Malis, M.D. Neurosurgeon Hollis Hills, New York REFERENCE 1. Malis LI. Arteriovenous malformations of the spinal cord. In: Youmans JR, ed. Neurological surgery. Philadelphia: WB Saunders, 1982:1850 –74.