Stereotactic radiosurgery for intramedullary spinal arteriovenous malformations

doi:10.1016/j.jocn.2015.12.005

Journal of Clinical Neuroscience

Volume 29, July 2016, Pages 162-167

https://doi.org/10.1016/j.jocn.2015.12.005 Get rights and content

Highlights

•
Spinal cord AVMs can present with recurrent hemorrhage or progressive ischemia.
•
Their size and location sometimes make embolization and/or microsurgical resection difficult.
•
We report 37 patients treated between 1997-2014 with CyberKnife stereotactic radiosurgery.
•
CyberKnife radiosurgery safely obliterates or significantly shrinks most intramedullary AVMs.

Abstract

Spinal cord arteriovenous malformations (AVM) are rare lesions associated with recurrent hemorrhage and progressive ischemia. Occasionally a favorable location, size or vascular anatomy may allow management with endovascular embolization and/or microsurgical resection. For most, however, there is no good treatment option. Between 1997 and 2014, we treated 37 patients (19 females, 18 males, median age 30 years) at our institution diagnosed with intramedullary spinal cord AVM (19 cervical, 12 thoracic, and six conus medullaris) with CyberKnife (Accuray, Sunnyvale, CA, USA) stereotactic radiosurgery. A history of hemorrhage was present in 50% of patients. The mean AVM volume of 2.3 cc was treated with a mean marginal dose of 20.5 Gy in a median of two sessions. Clinical and MRI follow-up were carried out annually, and spinal angiography was repeated at 3 years. We report an overall obliteration rate of 19% without any post-treatment hemorrhagic events. In those AVM that did not undergo obliteration, significant volume reduction was noted at 3 years. Although the treatment paradigm for spinal cord AVM continues to evolve, radiosurgical treatment is capable of safely obliterating or significantly shrinking most intramedullary spinal cord AVM.

Introduction

Spinal cord arteriovenous malformations (AVM) are a complex and somewhat heterogeneous disease spectrum, possibly involving dural vasculature at the nerve root, extra-dural vessels or the spinal cord vascular supply. They range from arteriovenous fistulae to more complex nidal malformations of the extra-dural and spinal vasculature.

Stereotactic radiosurgery has emerged over the last few decades as an option for treating cerebral AVM, along with traditional microsurgical and endovascular embolization techniques. Over 5000 patients have been treated with this technique since its introduction in 1972 [1]. Focal radiation is delivered by tuning the confocal geometry of the beams to a predefined lesion, causing progressive hyperplasia of the endothelial tissue of the AVM nidus. Over time, this results in progressive blood vessel occlusion and thrombosis [2]. In cerebral AVM measuring less than 2.5 cm, radiosurgery affords an obliteration rate of 80–85% [3], [4], [5], [6], [7], [8], [9].

Given its favorable obliteration outcomes for cerebral AVM, attention has been given to treating spinal cord AVM using stereotactic radiosurgery. Unlike cerebral AVM, multiple spinal cord AVM subtypes exist (Table 1), with typical classification into four distinct pathologic groups based on the location of the arteriovenous connections. Type I and Type IV are dural and perimedullary arteriovenous fistulae; these are often optimally treated with endovascular embolization and/or microsurgical resection. Among the variety of subtypes, those with a more compact nidus represent the optimal targets for radiosurgical treatment. Type III, also called juvenile-type or metameric AVM, are characterized by a large and diffuse intramedullary nidus, which can also extend into the extramedullary space. Juvenile-type AVM are less well-defined lesions, and thus are not optimal radiosurgical targets. Type II, also called glomus-type AVM, represent a compact vascular nidus and are often suitable radiosurgical targets. Embolization, with or without subsequent microsurgical resection, has previously been utilized as the cornerstone of glomus AVM treatment with good success [10].

Treating spinal cord AVM with radiosurgery was not feasible prior to the development of frameless, image-guided stereotaxy [11]. Spinal radiosurgery is dependent on the delivery of a large number of cross-fired radiation beams in order to effectively dose the delivery to specific targets in and around the spine. Radiosurgical treatment of AVM builds on prior work related to radiosurgical treatment paradigms for spinal tumors [11], [12], [13]. Although treatment of spinal tumors has proven to be successful, radiation toxicity to the spinal cord remains a concern. The ability to deliver multiple sessions of radiosurgery to an intramedullary vascular malformation has played a role in reducing this risk of neurotoxicity related to radiation delivery.

At Stanford, we employ the CyberKnife system (Accuray, Sunnyvale, CA, USA) for radiation delivery to patients with radiosurgically treatable lesions. We have since reported our spinal cord AVM radiosurgical experience, including an update [14], [15]. Here, we include more recent results.

Section snippets

Patient identification and selection

The Stanford University Medical Center, USA, offers CyberKnife radiosurgery to patients with Type II spinal cord AVM who are otherwise not candidates for microsurgical or endovascular embolization. Additionally, patients with Type III spinal cord AVM are considered candidates for radiosurgery if the vascular nidus is compact. In contrast, Type I and IV AVM are better treated with microsurgery or endovascular embolization. Low-flow vascular malformations, such as cavernous malformations and

Results

The Stanford experience has been twice reported in the literature [14], [15]. We present an updated review of spinal cord AVM treated with CyberKnife stereotactic radiosurgery.

Between 1996 and 2014, 37 patients underwent stereotactic radiosurgery for spinal cord AVM. Of 37 patients, 19 were female and 18 were male with a median age of 30 years. Spinal cord AVM distribution included cervical spine (19/37), thoracic spine (12/37), and the conus (6/30). The rate of hemorrhage at presentation was

Discussion

The use of CyberKnife radiosurgery to treat spinal cord AVM is continually evolving. Over time, improvements in imaging have made treatment of spinal cord AVM safe and accurate, and will continue to do so as techniques and imaging improve. High-resolution 3D images now provide a superior view of many spinal AVM compared to standard two-dimensional angiographic or planar imaging (Fig. 5). Algorithms that fuse 3D angiography images to either CT scans or MRI represent another advance in

Conclusions

CyberKnife radiosurgery appears to be an effective treatment for spinal cord AVM. The CyberKnife allows the flexibility of multi-session radiosurgery, which may reduce the risk of treatment. Additional challenges remain with respect to obtaining a better understanding of the tolerance of the spinal cord to radiosurgery, determining the role of radiosurgery in the general management of spinal AVM and the appropriate parameters for radiation delivery. The development of 3D angiography and the

Conflicts of Interest/Disclosures

The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication.

Acknowledgments

We thank Cheryl J. Christensen for assistance with the manuscript. We gratefully acknowledge support for this study from Craig and Kimberly Darian and Carol Bade to Dr. Steven Chang.

References (23)

P.M. Medin et al.
Spinal cord tolerance in the age of spinal radiosurgery: lessons from preclinical studies
Int J Radiat Oncol Biol Phys
(2011)
A. Sahgal et al.
Spinal cord tolerance for stereotactic body radiotherapy
Int J Radiat Oncol Biol Phys
(2010)
L. Steiner et al.
Stereotaxic radiosurgery for cerebral arteriovenous malformations. Report of a case
Acta Chir Scand
(1972)
S.D. Chang et al.
Stereotactic radiosurgery of arteriovenous malformations: pathologic changes in resected tissue
Clin Neuropathol
(1997)
O.O. Betti et al.
Stereotactic radiosurgery with the linear accelerator: treatment of arteriovenous malformations
Neurosurgery
(1989)
R.J. Coffey et al.
Stereotactic gamma radiosurgery for intracranial vascular malformations and tumors: report of the initial North American experience in 331 patients
Stereotact Funct Neurosurg
(1990)
F. Colombo et al.
Linear accelerator radiosurgery of cerebral arteriovenous malformations
Neurosurgery
(1989)
F. Colombo et al.
Linear accelerator radiosurgery of cerebral arteriovenous malformations: an update
Neurosurgery
(1994)
W.A. Friedman et al.
Linear accelerator radiosurgery for arteriovenous malformations
J Neurosurg
(1992)
G.K. Steinberg et al.
Stereotactic heavy-charged-particle Bragg-peak radiation for intracranial arteriovenous malformations
N Engl J Med
(1990)

L. Steiner

Radiosurgery in cerebral arteriovenous malformations

Cited by (18)

CyberKnife Radiosurgery for Spinal Intramedullary Arteriovenous Malformations: A Single-Center Experience
2023, World Neurosurgery
Intramedullary spinal arteriovenous malformation (ISAVM, glomus type) is a type of spinal cord arteriovenous malformation, which is a rare disease known often to have a complex vascular supply interfering with that of the spinal cord, and is in complex anatomical relations with cord structures and nerve roots. Though microsurgical and endovascular treatment has mainly been the standard options, in high-risk cases with these treatments, stereotactic radiotherapy (SRT) might be the option of choice.
We retrospectively reviewed 10 consecutive patients with ISAVM who received SRT using CyberKnife at the Japanese Red Cross Medical Center (Tokyo, Japan) from January 2011 to March 2022.
No case in this series suffered from hemorrhage after applying SRT. One case experienced neurological impairment 10 years after SRT, which we attributed to venous congestion due to the remaining lesion. No case of radiation myelopathy was observed in this series.
In one case, the nidus volume reduction and loss of flow voids were obvious, though improvement in the neurological outcome was not apparent. No radiological changes were observed in the other 9 patients.
Even in lesions without radiological changes, no hemorrhagic events were observed for an average period of 4 years. SRT may be a feasible option in treating ISAVM, especially for lesions in which microsurgical resection and endovascular treatment are inapplicable. To ascertain the safety and efficacy of this approach, further studies with more patients and longer follow-up is required.
Recurrence Rates Following Treatment of Spinal Vascular Malformations: A Systematic Review and Meta-Analysis
2023, World Neurosurgery
Spinal vascular malformations (SVMs), including arteriovenous malformations (AVMs) and arteriovenous fistulas (AVFs), are a varied group of vascular lesions that can be subclassified according to localization, vascular structure, and hemodynamics. Early intervention is necessary to halt progression of disease and minimize irreversible dysfunction. We sought to characterize initial treatment success and recurrence rates following interventional treatment of various types of SVMs.
A systematic review and meta-analysis were performed following the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines. SVMs were categorized into 4 groups: dural AVFs, perimedullary AVFs, intramedullary AVMs, and extradural-intradural AVMs (e.g., epidural, paraspinal). Initial occlusion, recurrence, and complication rates were compared using random-effects analysis.
There were 112 manuscripts included, with a total of 5626 patients with SVM. For treatment, 2735 patients underwent endovascular embolization, 2854 underwent surgical resection, and 37 underwent stereotactic radiosurgery. The initial treatment success and overall recurrence rates following surgical resection of all SVMs were 89.5% (95% CI: 80.5%–98.5%) and 2.3% (95% CI: 0.9%–3.7%), respectively. Those rates following endovascular embolization were 55.9% (95% CI: 30.3%–81.5%) and 27.7% (95% CI: 11.2%–44.2%), respectively. Higher rates of initial treatment success and lower rates of recurrence with surgery were observed in all subtypes compared to embolization. Overall complication rates were higher after embolization for each of the SVM categories.
Surgical resection of SVMs provided higher rates of initial complete occlusion and lower rates of recurrence than endovascular techniques. Attaining technical success through obliteration must still be weighed against clinical impact and natural history of the specific vascular malformation.
Spinal vascular malformations: Angiographic evaluation and endovascular management
2021, Handbook of Clinical Neurology
Citation Excerpt :
Partial treatment may target a dangerous feature, notably a ruptured SA. Stereotactic radiosurgery is uncommonly used for the treatment of SAVMs; a few recent studies appear to demonstrate its safety but report low rates of complete obliteration at this time (under 20%) (Kalani et al., 2016; Rashad et al., 2017; Zhan et al., 2019). The treatment goal for high-flow PmAVFs is a cure.
Spinal vascular malformations (SVM) are classified based on their location (intramedullary, perimedullary, radicular, extradural) and flow pattern (high-flow, low-flow, no arteriovenous shunt). High-flow SVMs are generally congenital lesions diagnosed in children and young patients without gender predominance. They present with hemodynamic disturbances, mass effect, or hemorrhages, but may also be discovered incidentally. Low-flow SVMs tend to be acquired lesions presenting in older men with progressive myelopathy caused by spinal venous hypertension. They are rarely associated with vascular syndromes but may accompany prothrombotic conditions. The sensitivity and specificity of conventional MRI are excellent for high-flow SVMs but poor for low-flow lesions, which are frequently diagnosed with extensive delays reducing the potential for favorable outcomes. The sensitivity of advanced MRI techniques remains unclear, notably for the detection of low-flow shunts without flow voids on conventional MRI. Catheter angiography remains the gold standard modality for the evaluation of the spinal vasculature and its disorders. SVMs can be treated by surgical or endovascular means. Initially plagued by high recurrence rates due to inadequate embolization material, endovascular techniques represent nowadays a valid alternative to surgery, thanks notably to the introduction of liquid embolic agents.
Adult Spinal Arteriovenous Malformations: Natural History and a Multicenter Study of Short-Term Surgical Outcomes
2019, World Neurosurgery
Spinal arteriovenous malformations (SAVMs) are a very rare and complex spinal cord pathology that require high clinical acumen to diagnose and treat. Management includes both nonoperative and operative paradigms. A review of the literature yields a paucity of data regarding the surgical outcomes of SAVMs, with the majority of data limited to single-center outcomes and/or small sample sizes. The purpose of this study was to use a multi-institutional international database to study the natural history of SAVMs.
We used the American College of Surgeons National Surgical Quality Improvement Program (ACS-NSQIP) database to select patients that underwent laminectomy for surgical excision of a SAVM between 2008 and 2017.
The data from 196 patients were studied (65.8% male, 34.2% female). A majority of cases were in the thoracic region (53.6%), followed by thoracolumbar (31.6%) and cervical (14.8%) regions. The mean age was 57.4 years and 52.5% patients were graded ASA class 3–5 before the operation. The mean operation time was 215 minutes, with a significantly lower operative time for thoracic arteriovenous malformations (195.6 minutes) when compared with cervical (266.6 minutes) and thoracolumbar (223.7 minutes). The mean length of hospital stay was 6.4 days. Patients had a 6.6% readmission rate and a 4.6% reoperation rate within 30 days.
This study presents the largest analysis of patients undergoing surgery for SAVMs and 30-day postoperative outcomes. Operative time differed based on SAVM location. The three most frequent complications (deep vein thrombosis, wound infection, and UTI) occurred at rates of 3.6% or less.
Stereotactic radiosurgery and fractionated radiotherapy for spinal arteriovenous malformations – A systematic review of the literature
2019, Journal of Clinical Neuroscience
Citation Excerpt :
As with type I AVFs, treatment of type IV perimedullary AVFs can also be performed with transarterial embolization of microsurgical disconnection, the optimal choice often depending on the unique arterial anatomy of each AVF. As summarized here, stereotactic radiosurgery and fractionated radiotherapy for spinal arteriovenous malformations have been the subject of only a few retrospective reports (Table 1) [4–11,14] and there have been no published prospective studies. The vast majority of patients included in this systematic review (94.8%) were treated with a linear accelerator and the majority of those using the CyberKnife radiosurgery system.
Spinal arteriovenous malformations (AVMs) comprise a group of complex vascular lesions whose treatment with microsurgery or transarterial embolization can be challenging. Stereotactic radiosurgery is a well-established treatment for intracranial AVMs, and spinal radiosurgery and fractionated radiotherapy are common treatments for spinal tumors of both primary and metastatic origin. The use of radiosurgery and fractionated radiotherapy for the treatment of spinal arteriovenous malformations, however, has been infrequently reported. Spinal stereotactic radiosurgery is emerging as a promising option for the treatment of these lesions. We conducted a systematic review of English language articles reporting one or more cases of spinal radiosurgery or fractionated radiotherapy for the treatment of spinal arteriovenous fistulas (AVFs) or arteriovenous malformations. Eight unique studies comprising 64 patients were identified. All treated lesions consisted primarily of spinal AVMs, either intramedullary or metameric. Most were treated with CyberKnife technology. Marginal doses in the most current studies ranged from 18 to 21 Gy given over 2–4 fractions. In aggregate, good outcomes were reported in 92.2% with no instances of post-treatment hemorrhage over a mean follow-up time of 46.8 months. Angiographic follow-up showed the nidus to be obliterated in 16%, decreased in 44.6%, and unchanged in 39.3%. Stereotactic radiosurgery for spinal arteriovenous malformations holds promise as a safe and potentially effective option in the treatment of these rare but complex lesions.
Technical aspects and indications of extracranial stereotactic radiotherapy
2018, Cancer/Radiotherapie
La radiothérapie stéréotaxique extracrânienne s’est considérablement développée ces dernières années et tient désormais une part importante dans les alternatives thérapeutiques à proposer aux patients atteints de cancer. Elle offre des possibilités qui ont progressivement amené les praticiens à reconsidérer la stratégie thérapeutique, par exemple en cas de récidive locale en territoire irradié ou de maladie oligométastatique. La littérature sur le sujet est riche mais il n’existe pas encore à ce jour de véritables consensus sur les indications thérapeutiques. Cela est en grande partie lié au fait qu’il n’existe que peu d’étude prospective randomisée ayant évalué cette technique avec un recul suffisant. Nous proposons ainsi une revue de la littérature sur l’aspect technique et sur les indications de la radiothérapie stéréotaxique extracrânienne.
Extracranial stereotactic radiotherapy has developed considerably in recent years and is now an important part of the therapeutic alternatives to be offered to patients with cancer. It offers opportunities that have progressively led physicians to reconsider the therapeutic strategy, for example in the case of local recurrence in irradiated territory or oligometastatic disease. The literature on the subject is rich but, yet, there is no real consensus on therapeutic indications. This is largely due to the lack of prospective, randomized studies that have evaluated this technique with sufficient recoil. We propose a review of the literature on the technical aspects and indications of extracranial stereotactic radiotherapy.

View all citing articles on Scopus

View full text

Clinical StudyStereotactic radiosurgery for intramedullary spinal arteriovenous malformations

Highlights

Abstract

Introduction

Section snippets

Patient identification and selection

Results

Discussion

Conclusions

Conflicts of Interest/Disclosures

Acknowledgments

Int J Radiat Oncol Biol Phys

Int J Radiat Oncol Biol Phys

Stereotaxic radiosurgery for cerebral arteriovenous malformations. Report of a case

Acta Chir Scand

Stereotactic radiosurgery of arteriovenous malformations: pathologic changes in resected tissue

Clin Neuropathol

Stereotactic radiosurgery with the linear accelerator: treatment of arteriovenous malformations

Neurosurgery

Stereotactic gamma radiosurgery for intracranial vascular malformations and tumors: report of the initial North American experience in 331 patients

Stereotact Funct Neurosurg

Linear accelerator radiosurgery of cerebral arteriovenous malformations

Neurosurgery

Linear accelerator radiosurgery of cerebral arteriovenous malformations: an update

Neurosurgery

Linear accelerator radiosurgery for arteriovenous malformations

J Neurosurg

Stereotactic heavy-charged-particle Bragg-peak radiation for intracranial arteriovenous malformations

N Engl J Med

Radiosurgery in cerebral arteriovenous malformations

Clinical Study
Stereotactic radiosurgery for intramedullary spinal arteriovenous malformations