Surgical and Endovascular Treatment of Pediatric Spinal Arteriovenous Malformations
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1 Surgical and Endovascular Treatment of Pediatric Spinal Arteriovenous Malformations M. Yashar S. Kalani, Azam S. Ahmed, Nikolay L. Martirosyan, Katharine Cronk, Karam Moon, Felipe C. Albuquerque, Cameron G. McDougall, Robert F. Spetzler, Ruth E. Bristol Key words Arteriovenous malformation Embolization Endovascular Microsurgery Pediatrics Spine Abbreviations and Acronyms AVM: Arteriovenous malformation DSA: Digital subtraction angiography KTW: Klippel-Trènaunay-Weber syndrome SAH: Subarachnoid hemorrhage WHO: World Health Organization Division of Neurological, Barrow Neurological Institute, St. Joseph s Hospital and Medical Center, Phoenix, Arizona, USA To whom correspondence should be addressed: Ruth E. Bristol, M.D. [ neuropub@chw.edu] Citation: World Neurosurg. (2012) 78, 3/4: DOI: /j.wneu Journal homepage: Available online: /$ - see front matter 2012 Elsevier Inc. All rights reserved. OBJECTIVE: Pediatric spinal arteriovenous malformations (AVMs) are rare and complex lesions to treat. There are few reports of the endovascular and microsurgical treatment of these lesions in the pediatric population, and the treatment outcomes of these patients are not well described. The aim of this study was the clinical and radiographic outcomes of spinal AVMs in pediatric patients treated via endovascular and microsurgical modalities. METHODS: We identified nine children (5 boys, 4 girls; average age 11 years, range 3 17 years) treated for spinal AVMs between 1998 and Their charts were reviewed. RESULTS: Spinal AVMs most frequently involved the thoracic spinal cord. Four patients had associated Klippel-Trènaunay-Weber syndrome and one had hereditary hemorrhagic telangiectasia. There were two intramedullary, four conus medullaris, and three mixed extradural-intradural lesions. The most common presenting signs and symptoms were subarachnoid hemorrhage (n 3) and paraparesis (n 5). Endovascular intervention was used exclusively in two patients, and combined endovascular and microsurgical intervention was used in four patients. was the sole treatment in three patients with excellent results. There were two treatment-related complications: one case of subarachnoid hemorrhage and one case of scrotal swelling. The mean follow-up was 28.5 months and the median was 8 months (range, 1 65 months). The mean pretreatment World Health Organization (WHO)/Zubrod score was 2.4 (range, 1 4), and the mean post-treatment score was 1.4 (range, 0 4). One patient (11%) had a recurrence. CONCLUSIONS: Pediatric spinal AVMs require complex combined microsurgical and endovascular techniques to achieve favorable outcomes. INTRODUCTION In the past 50 years, our understanding of spinal arteriovenous lesions has increased exponentially thanks to the development of spinal angiography and the increasing ability of neurosurgical centers to treat these lesions by either endovascular or microsurgical means. In addition to the almost ubiquitous four-point grading system described in classic literature (11, 15), several classifications schemes have been proposed including those by Borden et al. (8), Niimi and Berenstein (23), Bao and Ling (5), Rosenblum et al. (31), and the senior author (R.F.S.) (21, 34). These classification systems are based on the pathophysiology, imaging, anatomy, and intraoperative reports of spinal arteriovenous malformations (AVMs). Spinal AVMs and arteriovenous fistulas are rare in the pediatric population, but are as complicated as their adult counterparts. Reports of individual cases in children (2, 3, 6, 7, 9, 14, 16-18, 20, 26-28, 37-40) culminated in the publication of several contemporary series (12, 13, 29, 36) from high-volume vascular centers. The presentation of these lesions in children is similar to that in adults. The lesions often manifest as congestive or compressive myelopathy, back pain, and, less acutely, as murmurs or pulsating paraspinal masses on examination. Less common presentations include scoliosis, gait disturbance, and congestive heart failure. Spinal AVMs have also been associated with inherited disorders such as hereditary hemorrhagic telangiectasia (28), familial cerebral cavernous hemangiomas (18), familial cutaneous hemangiomas (20), pulmonary AVMs (32), and Klippel-Trenaunay-Weber (KTW) (1, 19, 30). Given the coincidence of spinal vascular malformations with syndromal disorders, a complete workup to exclude syndromic causes of vascular malformations is warranted. Given the relatively sparse literature on the treatment and outcome of pediatric spinal AVMs, we reviewed our institutional series of nine pediatric patients treated by microsurgical resection and endovascular intervention. MATERIALS AND METHODS We searched a prospectively maintained surgical database for pediatric patients who underwent microsurgical and/or endovascular treatment for spinal AVMs from 1998 to Nine patients (5 boys, 4 girls; male-to-female ratio, 5:4; mean WORLD NEUROSURGERY, DOI: /j.wneu
2 Table 1. Clinical Summary of Nine Pediatric Patients with Spinal AVMs WHO/Zubrod Score Recurrence/ Residual Last Follow-up Before Length of Follow-up (months) Presenting Symptoms Treatment Complications Associated Syndrome Type of AVM Patient Sex/Age Location Scrotal swelling No 1 M/3 L3 KTW Conus medullaris Heart failure Transarterial embolization 2 F/5 T10-L2 HHT Conus medullaris Paraparesis None No 3 M/9 C7-T1 KTW Intramedullary Arm numbness None None SAH None Transarterial embolization 4 M/10 T12-L2 KTW Extradural/intradural Paraparesis Loss of bowel and bladder function Paraplegia None Residual (re-embolized) Transarterial 5 F/12 T11-L3 Conus medullaris SAH Seizure Paraparesis None None 6 F/12 C3-C5 Extradural/intradural Paraparesis Transarterial None None 7 M/13 T10-L1 Intramedullary Paraparesis Transarterial None None 8 M/14 T10-L1 KTW Conus medullaris SAH Transarterial 9 F/17 C1-C2 Intramedullary SAH None Recurrence at C1-C5 (observed) KTW, Klippel-Trenaunay-Weber; HHT, hereditary hemorrhagic telangiectasia; SAH, subarachnoid hemorrhage; AVM, arteriovenous malformation. age 11 years, range 3 17 years) were identified. All patients were treated by the neurovascular team (R.F.S., C.G.M., and F.C.A.) at the Barrow Neurological Institute, St. Joseph s Hospital, Phoenix, Arizona. These patients had not received prior treatment. The patients hospital and office records were reviewed retrospectively for age at admission, presenting symptoms, type and location of lesions, treatment, complications, and clinical outcomes at last followup. Lesions were classified based on the Spetzler spinal AVM grading scale (21, 34). Outcomes were based on the World Health Organization/Zubrod score (24). Clinical follow-up (mean, 28.5 months; median, 8 months; range, 1 65 months) was available for all nine patients. RESULTS All patients presented after becoming symptomatic from their spinal AVM (Table 1). Three patients (33%) presented after subarachnoid hemorrhage (SAH). Five patients (56%) presented with paraparesis. Other presenting symptoms included paraplegia, heart failure, and loss of bowl and bladder function. Four patients had KTW syndrome and one patient had hereditary hemorrhagic telangiectasia. Types of AVMs Four patients (44%) had a conus medullaris spinal AVM. Three patients (33%) had an intramedullary lesion, whereas two patients (22%) had an extradural-intradural lesion. The lesions were exclusively cervical in three patients (33%), thoracolumbar in five (56%), and exclusively lumbar in one patient (11%). Treatment Altogether, the 9 patients underwent 13 procedures (Table 1). The three patients (33%) treated solely by microsurgical technique had laminectomies, followed by dissection and resection of the lesions to obtain decompression of the neurovascular compartments. Two patients (22%) were treated by endovascular obliteration of the feeding vessels to the AVM. In four patients (44%), endovascular obliteration of the feeding vessels of the AVM was combined with microsurgical decom- WORLD NEUROSURGERY 78 [3/4]: , SEPTEMBER/OCTOBER
3 pression and resection of the embolized lesions. After treatment, all patients were evaluated by angiography to ensure obliteration of the lesions. In all patients, the embolizations were performed through a transarterial route. Both ethylene vinyl alcohol copolymer (Onyx; ev3, Irvine, California, USA) and n-butyl cyanoacrylate were used as embolizing agents. Outcomes We obtained angiographic obliteration in eight of the nine patients (89%). The single case with residual was treated with repeat embolization, which resulted in obliteration of the lesion. There were no deaths in the perioperative period. All patients examinations were stable postoperatively. Perioperative complications were noted in 2 patients after 13 procedures (Table 1). One patient (case 4) suffered procedure-related SAH and required an extended stay in the intensive care unit. This patient was severely disabled before treatment and had improved considerably at last follow-up. After angiography another patient (case 1) suffered from scrotal swelling (this was attributed to hematoma), which improved during the postoperative period, and the patient was asymptomatic at discharge. No other patients suffered transient deterioration post-procedurally or after surgery. Based on the WHO/Zubrod score, all patients had improved or stayed the same at last follow-up (Table 1). The mean before and after treatment WHO/Zubrod scores were 2.4 and 1.4, respectively. On follow-up imaging, one patient (case 9) had developed a recurrence; given the patient s poor functional status, she was followed closely. Case Examples Case 3. After several months of exhibiting signs of progressive arm numbness, a 9-year-old boy with a history of KTW syndrome was brought for evaluation. Magnetic resonance angiography revealed a large intramedullary spinal AVM at C7-T1 (Figure 1A). The day before the scheduled surgical resection of the lesion, the patient underwent selective angiography. The angiogram showed opacification of the anterior spinal artery when contrast material was injected into terminal feeders of the vascular malformation. Given that opacification of the anterior spinal artery reflects flow into Figure 1. (A) Case 3. Sagittal T 1 - and T 2 -weighted magnetic resonance angiograms and spinal angiogram show an arteriovenous malformation at C7-T1. (B) The patient underwent surgical resection of the lesion with excellent resection and decompression of the spinal cord. Used with permission from Barrow Neurological Institute. the artery, and the increased risk of the embolization material causing occlusion of the artery with devastating sequela, it was thought that sacrifice of the arterial pedicle arising from this artery would lead to an unacceptably high risk of neurological impairment; thus, the procedure was aborted. The patient subsequently underwent laminectomy and resection of the spinal AVM (Figure 1B). At last follow-up, his arm numbness had resolved completely and he was asymptomatic. Case 6. A 12-year-old girl with a 3-month history of progressive weakness and numbness below C5 presented with arm and leg pain. On examination she had contractures of the triceps and was flaccid at the grips and dorsal interossei. The patient was not antigravity (2/5 in strength) at hip flexors or knee extensors, but was strong distally (4 4 /5 in strength). Magnetic resonance imaging of the cervical spine revealed an extradural-intradural AVM extending from the bottom of C3 to the top of C6 (Figure 2A) WORLD NEUROSURGERY, DOI: /j.wneu
4 Figure 2. (A) Case 6. Sagittal T 2 -weighted magnetic resonance images show a large spinal arteriovenous malformation extending from the bottom of the C3 to the top of the C6 vertebra. The corresponding axial cuts of the spinal cord are also presented. (B) Angiogram reveals a tangle of vessels corresponding to the arteriovenous malformation. (C) Selective catheterization of distal vessels allows for visualization and controlled embolization of feeders to the vascular malformations. (D) After embolization with Onyx and n-butyl cyanoacrylate, the lesion was resected through a posterior approach. (continues) WORLD NEUROSURGERY 78 [3/4]: , SEPTEMBER/OCTOBER
5 Angiography revealed the lesion with its prominent feeders and tangle of vessels (Figure 2B). Superselective angiography performed in the anterior, posterior, and lateral projections revealed that the thyrocervical trunk supplied the malformation nidus as well as retrograde filling of the left vertebral artery through a muscular branch (Figure 2C). Onyx was used to embolize the vascular pedicle as well as the branch off the thyrocervical trunk that fed the malformation. This resulted in a decrement in the rapidity at which the draining vein was filled. Other feeders supplying the nidus were similarly identified and sequentially embolized using Onyx. The angiography taken after embolization with an injection into the right thyrocervical trunk demonstrated significant reduction in flow to the malformation and slowing of the transit of contrast through the AVM (Figure 2D). There was also notable flow through the anterior spinal artery from the nidus and early filling of the large draining veins of the AVM. A total of 0.8 ml of Onyx was administered during 61 minutes of fluoroscopy time. After the procedure, the patient s status was unchanged on examination. On day 1 after the procedure, she underwent laminectomy and resection of the embolized lesion, with decompression of the spinal cord (Figure 2E). Postoperative angiography with injection of the right vertebral artery and thyrocervical trunk showed no evidence of any early draining veins or nidus. Postoperatively, her neurological status began to improve, and she was discharged from the hospital ambulating with assistance. At last follow-up, the patient was able to perform her daily tasks with minimal assistance. DISCUSSION The management of spinal vascular malformations depends on the type of lesion and technical capabilities of the treating institution. In general, we advocate combined endovascular and open vascular treatment of spinal vascular lesions because preoperative embolization greatly facilitates surgical resection. Given the scarcity of data on spinal AVMs in the pediatric population, we extrapolated the outcomes from the relatively large experience with the treatment of adult spinal AVMs to the pediatric population. We begin our discussion of the treatment of pediatric spinal vascular malformations with some pathology-specific considerations and follow with our methodology used in some of our patients. Treatment by Pathology Intradural-Intramedullary. Although surgical resection remains the gold standard for treating intradural-intramedullary AVMs (10, 34), embolization alone (4) or in combination with surgery has been shown to provide acceptable results. Typically, a posterior or posterolateral surgical approach is used, but an anterior approach may be used in selected cases (10, 22, 42). We do not advocate chasing vascular loops of AVM that may dive into the spinal cord parenchyma; we believe that it is better to truncate vessels embedded in the parenchyma at the pial surface than to seek deeper loops that may cause neurologically devastating injury. Extradural-Intradural. These challenging lesions involve neural structures, bone, and soft tissue along the affected spinal level and are usually impossible to resect completely, although a few cases have been reported (22, 35, 41). The goals of treatment are the disconnection of large feeding vascular pedicles (thereby minimizing vascular steal and venous hypertension) and decompression of mass effect along the nerve roots and spinal cord (15, 22, 23, 25, 35). Conus Medullaris. These AVMs are treated with combined endovascular and microsurgical approach. Angiography allows for identification of the anterior and posterior spinal arteries and embolization of feeders from these vessels. The venous vasculature associated with conus medullaris AVMs are vastly dilated and surgical decompression and resection through a posterior approach can relieve neurological symptoms associated with conus AVMs. In our experience, aggressive combined treatment can result in good outcomes (34). Multimodality Treatment of Pediatric Spinal AVMs The Role of Angiography. Spinal angiography for embolization of AVMs requires keen attention to detail. All potential feeding arteries must be evaluated. Often, arteries distant to the nidus may supply the vascular malformation. Each arterial feeding pedicle is assessed individually for supply to the AVM nidus through microcatheter digital subtraction angiography (DSA). As important as parsing out the inflow, nidus, and outflow is determining which vessels must be preserved. The anterior spinal artery must be identified, as well as any anastomotic radiculomedullary vessels. In the cervical region, anastomoses often exist between external carotid artery branches and the vertebral artery. Furthermore, anastomoses with vessels of the contralateral cervical cerebral circulation may be present. If such anastomoses are identified, great care must be exercised during embolization to avoid inadvertent embolization by defining clear landmarks and stopping points. Alternatively, these channels can be occluded with coils or embolic agents to ensure embolic material does not reflux into normal arteries. When the operator is certain that such pathways are no longer present, the pedicles are assessed for the presence of en passage vessels. If possible, the microcatheter is navigated distal to these normal branches. If this is not possible or if these branches are at risk of being embolized due to reflux of embolic material, provocative testing may be performed. The Role of Provocative Testing. Provocative testing requires the patient not only to be awake but also minimally sedated to participate in frequent neurological assessments. Once the microcatheter is positioned as close to the nidus as possible, sodium amytal or lidocaine is infused and the patient is assessed for neurological deficits. It is important that amytal and lidocaine be mixed with contrast and that it is injected during continuous DSA to assess for reflux. The optimal injection rate is determined before provocative testing and embolization with multiple hand injections and tailored to avoid reflux. If the patient develops deficits, the test is considered positive and embolization should not be performed at this microcatheter position. If deficits are not elicited, the test is considered negative and embolization may proceed. Important, if multiple pedicles are embolized and there are significant changes in the flow through the AVM, provocative testing may be repeated to ensure safety of embolization of the remaining pedicles. The Role of Embolization. Embolization of the AVM is performed once the endovascular dissection of the AVM with microcatheter angiography and provocative testing are complete. Embolization can be per WORLD NEUROSURGERY, DOI: /j.wneu
6 some cases and depends on which component of the AVM is causing the patient s symptoms, on the thoroughness of embolization, and on the flow dynamics of the AVM. In particular, it is prudent not to resect completely embolized components of the AVM if doing so would require additional pial dissection or if resection results in changes in spinal monitoring. Specifically, in cases of large superficial AVMs with diving vessel loops that penetrate the spinal cord, we do not advocate following these diving vessels because the risk of causing neurological injury outweighs the benefit of complete resection. In our hands, this technique has allowed for the resection of complex AVMs with minimal morbidity and often improvement in premorbid deficits. The Role of Postoperative Angiography. Angiographic confirmation of obliteration of the AVM is mandatory after resection. Frequent follow-up should be performed initially, with the interval of radiographic and clinical surveillance lengthening if recurrence does not occur. Any new neurological symptoms or signs should be thoroughly investigated with magnetic resonance imaging and catheter angiography as soon as possible. Figure 2. (continued) (E) Postoperative sagittal T 2 -weighted magnetic resonance image confirms gross total resection of the lesion and decompression of the spinal cord. The corresponding axial cuts of the spinal cord are also presented. Used with permission from Barrow Neurological Institute. The Role of Radiation. Stereotactic radiosurgery has been suggested as a treatment modality for spinal AVMs (33). However, we do not advocate its use, given the life expectancy of pediatric patients and the relatively small size of their spinal cord. formed with either n-butyl cyanoacrylate or Onyx. The embolization techniques have been well described elsewhere (1, 39). In many cases the feeding arteries can be embolized with sparing of the draining veins. Intraoperatively, indocyanine green videoangiography can be used to identify the draining vein for resection. At our institution, all embolization procedures are performed using neurological monitoring of somatosensory-evoked potentials, motorevoked potentials, and brainstem auditoryevoked potentials. Although the merit of neurophysiologic monitoring is debated, it often provides valuable information. As with any diagnostic modality, these data need to be interpreted in the context of the clinical situation. A significantly decreased amplitude or increased latency should prompt an investigation of potential causes for such changes. The Role of Surgical Resection. After embolization, the AVM is surgically resected. We frequently use a posterior or posterolateral approach to these lesions. Indocyanine green videoangiography is helpful in correlating the preoperative DSA with the intraoperative anatomy and thereby guiding resection. Complete surgical extirpation of AVMs should be performed when possible. The classic mantra of complete resection, often with disastrous consequences, has resulted in many spinal AVMs being deemed unresectable based on previous bad outcomes. At our institution, each AVM is evaluated and treated using an individualized approach. Partial resection is performed in CONCLUSIONS During the past 12 years, we have treated nine children for spinal AVMs, most of which were thoracic. Several group of investigators, including our own, have noted an association between these lesions and KTW syndrome (1, 19, 30). Four of our patients had KTW syndrome and a spinal AVM. Given the association between spinal AVMs and arteriovenous fistulas, we advocate workup for syndromic causes in the pediatric population. There were no deaths in our series, and the two treatment-related complications of SAH and scrotal swelling resolved without long-term sequelae. At last follow-up all of our patients had stable or improved WHO/Zubrod scores. Our experience with the treatment of spinal AVMs in children suggests that combined endovascular and open vascular treat- WORLD NEUROSURGERY 78 [3/4]: , SEPTEMBER/OCTOBER
7 ment of these lesions is safe and effective with long-lasting resolution of symptoms and improved functioning of patients. Nonetheless, despite progress in treatment modalities, the management of pediatric spinal AVMs remains challenging. REFERENCES 1. Alexander MJ, Grossi PM, Spetzler RF, McDougall CG: Extradural thoracic arteriovenous malformation in a patient with Klippel-Trenaunay-Weber syndrome: case report. Neurosurgery 51: , Alonso Fernandez L, Nzau M, Ventureyra E: Spinal intradural arteriovenous fistula with unusual presentation: case report and literature review. Childs Nerv Syst 24: , Anson JA, Spetzler RF: Surgical resection of intramedullary spinal cord cavernous malformations. J Neurosurg 78: Ausman JI, Gold LH, Tadavarthy SM, Amplatz K, Chou SN: Intraparenchymal embolization for obliteration of an intramedullary AVM of the spinal cord. Technical note. 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Received July 07, 2011; accepted October 21, 2011; published online 01 November 2011 Citation: World Neurosurg. (2012) 78, 3/4: DOI: /j.wneu Journal homepage: Available online: /$ - see front matter 2012 Elsevier Inc. All rights reserved WORLD NEUROSURGERY, DOI: /j.wneu
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