Risk of hemorrhage from an arteriovenous malformation confirmed to have been obliterated on angiography after stereotactic radiosurgery

Restricted access

Object. Radiosurgery has been widely adopted for the treatment of cerebral arteriovenous malformations (AVMs) in which the practical endpoint is angiographic evidence of obliteration, presumed to be consistent with elimination of the risk of hemorrhage. To test this unverified assumption, the authors followed 236 radiosurgery-treated AVMs between 1 and 133 months (median 77 months) after angiographic evidence of obliteration.

Methods. Four patients experienced hemorrhage between 16 and 51 months after angiographic confirmation of AVM obliteration, and two underwent resection. The histological findings in these patients showed occlusion of the AVM by thickening of the intimal layer with dense hyalinization as well as a small amount of residual AVM vessels and a tiny vasculature. The risks of hemorrhage from these presumaby obliterated AVMs were 0.3% for the annual bleeding risk and 2.2% for the cumulative risk over 10 years. Continuous enhancement of the nidus on computerized tomography (CT) or magnetic resonance (MR) imaging was the only significant factor positively associated with hemorrhage in the statistical analysis (p = 0.0212).

Conclusions. Because the study was based on limited follow-up data, its significance for defining predictive features of hemorrhage after angiographic evidence of obliteration is still indeterminable. Nevertheless, disappearance of the AVM on angiography after radiosurgery does not always indicate total elimination of the disease, especially when CT or MR imaging continues to demonstrate an enhancing lesion. The authors therefore recommend continual follow up even after evidence of AVM obliteration on angiography.

Article Information

Address reprint requests to: Masahiro Shin, M.D., Ph.D., Department of Neurosurgery, University of Tokyo Hospital, 7–3–1 Hongo, Bunkyo-ku, Tokyo, 113–8655, Japan. email: shinmasa@ka2.so-net.ne.jp.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Case 1. Left internal carotid artery angiogram (A, lateral view) demonstrating a left frontal AVM which was treated with GKS. Obliteration of the AVM was confirmed on a later angiogram (B), although the AVM (arrow) continued to enhance on this MR image (C). This patient experienced acute intracerebral hemorrhage 16 months after obliteration. Intraoperative photograph (D) showing a pale and shrunken draining vein (arrow) and a solidified nidus (arrowhead).

  • View in gallery

    Case 2. An axial enhanced CT scan (A) and a right vertebral artery angiogram (B, anteroposterior view) revealing an AVM (arrow in A) in the right occipital lobe. The lesion was treated with GKS and a cerebral angiogram revealed complete obliteration (C). This patient experienced acute intracerebral hemorrhage 38 months after evidence of AVM obliteration. She was observed conservatively and the degenerated nidus continuously enhanced on MR imaging (arrow in D). Twenty-nine months later, it was accompanied by a slowly enlarging cyst (arrowhead in D), and the nidus was resected 38 months after the hemorrhage.

  • View in gallery

    Surgical specimen of the resected AVM in Case 1 showing a blisterlike component (A, arrowhead) and a hematoma (A, arrow). A similar blisterlike piece was also found in Case 2 (B). Histological examinations of these specimens showed small endothelial cell—lined channels containing erythrocytes within the area of hyalinization (C, Case 1), closure of the vascular lumen by thickening of the intimal layer in the majority of the parts, and a patent nidus (D, Case 2). H & E (C and D), original magnifications × 100 (C) and × 40 (D).

References

  • 1.

    Del Curling O JrKelly DL JrElster ADCraven TE: An analysis of the natural history of cavernous angiomas. J Neurosurg 75:7027081991Del Curling O Jr Kelly DL Jr Elster AD Craven TE: An analysis of the natural history of cavernous angiomas. J Neurosurg 75:702–708 1991

  • 2.

    Fleetwood IGSteinberg GK: Arteriovenous malformations. Lancet 359:8638732002Fleetwood IG Steinberg GK: Arteriovenous malformations. Lancet 359:863–873 2002

  • 3.

    Hartmann AStapf CHofmeister CMohr JPSciacca RRStein BMet al: Determinants of neurological outcome after surgery for brain arteriovenous malformation. Stroke 31:236123642000Hartmann A Stapf C Hofmeister C Mohr JP Sciacca RR Stein BM et al: Determinants of neurological outcome after surgery for brain arteriovenous malformation. Stroke 31:2361–2364 2000

  • 4.

    Kadota OSakaki SKumon YOhta SKohno K: Large cystic cavernous angioma of the cerebellum—case report. Neurol Med Chir 34:7687721994Kadota O Sakaki S Kumon Y Ohta S Kohno K: Large cystic cavernous angioma of the cerebellum—case report. Neurol Med Chir 34:768–772 1994

  • 5.

    Kihlström LGuo WYKarlsson BLindqvist CLindquist M: Magnetic resonance imaging of obliterated arteriovenous malformations up to 23 years after radiosurgery. J Neurosurg 86:5895931997Kihlström L Guo WY Karlsson B Lindqvist C Lindquist M: Magnetic resonance imaging of obliterated arteriovenous malformations up to 23 years after radiosurgery. J Neurosurg 86:589–593 1997

  • 6.

    Kondziolka DLunsford LDKestle JR: The natural history of cerebral cavernous malformations. J Neurosurg 83:8208241995Kondziolka D Lunsford LD Kestle JR: The natural history of cerebral cavernous malformations. J Neurosurg 83:820–824 1995

  • 7.

    Kurita HKawamoto SSasaki TShin MTago MTarahara Aet al: Results of radiosurgery for brain stem arteriovenous malformations. J Neurol Neurosurg Psychiatry 68:5635702000Kurita H Kawamoto S Sasaki T Shin M Tago M Tarahara A et al: Results of radiosurgery for brain stem arteriovenous malformations. J Neurol Neurosurg Psychiatry 68:563–570 2000

  • 8.

    Levy EINiranjan AThompson TPScarrow AMKondziolka DFlickinger JCet al: Radiosurgery for childhood intracranial arteriovenous malformations. Neurosurgery 47:8348422000Levy EI Niranjan A Thompson TP Scarrow AM Kondziolka D Flickinger JC et al: Radiosurgery for childhood intracranial arteriovenous malformations. Neurosurgery 47:834–842 2000

  • 9.

    Lindqvist MKarlsson BGuo WYKihlström LLippitz BYamamoto M: Angiographic long-term follow-up data for arteriovenous malformations previously proven to be obliterated after gamma knife radiosurgery. Neurosurgery 46:8038102000Lindqvist M Karlsson B Guo WY Kihlström L Lippitz B Yamamoto M: Angiographic long-term follow-up data for arteriovenous malformations previously proven to be obliterated after gamma knife radiosurgery. Neurosurgery 46:803–810 2000

  • 10.

    Lunsford LDKondziolka DFlickinger JCBissonette DJJungreis CAMaitz AHet al: Stereotactic radiosurgery for arteriovenous malformations of the brain. J Neurosurg 75:5125241991Lunsford LD Kondziolka D Flickinger JC Bissonette DJ Jungreis CA Maitz AH et al: Stereotactic radiosurgery for arteriovenous malformations of the brain. J Neurosurg 75:512–524 1991

  • 11.

    Mast HYoung WLKoennecke HCSciacca RROsipov APile-Spellmen Jet al: Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation. Lancet 350:106510681997Mast H Young WL Koennecke HC Sciacca RR Osipov A Pile-Spellmen J et al: Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation. Lancet 350:1065–1068 1997

  • 12.

    Ogilvy CSStieg PEAwad IBrown RD JrKondziolka DRosenwasser Ret al: AHA Scientific Statement: Recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. Stroke 32:145814712001Ogilvy CS Stieg PE Awad I Brown RD Jr Kondziolka D Rosenwasser R et al: AHA Scientific Statement: Recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council American Stroke Association. Stroke 32:1458–1471 2001

  • 13.

    Ondra SKTroupp HGeorge EDSchwab K: The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 73:3873911990Ondra SK Troupp H George ED Schwab K: The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 73:387–391 1990

  • 14.

    Pik JHTMorgan MK: Microsurgery for small arteriovenous malformations of the brain: results in 110 consecutive patients. Neurosurgery 47:5715772000Pik JHT Morgan MK: Microsurgery for small arteriovenous malformations of the brain: results in 110 consecutive patients. Neurosurgery 47:571–577 2000

  • 15.

    Pollock BEBrown RD Jr: Management of cysts arising after radiosurgery to treat intracranial arteriovenous malformations. Neurosurgery 49:2592652001Pollock BE Brown RD Jr: Management of cysts arising after radiosurgery to treat intracranial arteriovenous malformations. Neurosurgery 49:259–265 2001

  • 16.

    Riva DPantaleoni CDevoti MLindquist CSteiner LGiorgi C: Radiosurgery for cerebral AVMs in children and adolescents: the neurobehavioral outcome. J Neurosurg 86:2072101997Riva D Pantaleoni C Devoti M Lindquist C Steiner L Giorgi C: Radiosurgery for cerebral AVMs in children and adolescents: the neurobehavioral outcome. J Neurosurg 86:207–210 1997

  • 17.

    Sasaki TKurita HSaito IKawamoto SNemoto STerahara Aet al: Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101 cases. J Neurosurg 88:2852921998Sasaki T Kurita H Saito I Kawamoto S Nemoto S Terahara A et al: Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101 cases. J Neurosurg 88:285–292 1998

  • 18.

    Shin MMaruyama KKurita HKawamoto STago MTerahara Aet al: Analysis of nidus obliteration rates after gamma knife surgery for arteriovenous malformations based on long-term follow-up data: the University of Tokyo experience. J Neurosurg 101:18242004Shin M Maruyama K Kurita H Kawamoto S Tago M Terahara A et al: Analysis of nidus obliteration rates after gamma knife surgery for arteriovenous malformations based on long-term follow-up data: the University of Tokyo experience. J Neurosurg 101:18–24 2004

  • 19.

    Siddiqui AAJooma R: Neoplastic growth of cerebral cavernous malformation presenting with impending cerebral herniation: a case report and review of the literature on de novo growth of cavernomas. Surg Neurol 56:42452001Siddiqui AA Jooma R: Neoplastic growth of cerebral cavernous malformation presenting with impending cerebral herniation: a case report and review of the literature on de novo growth of cavernomas. Surg Neurol 56:42–45 2001

  • 20.

    Spetzler RFMartin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:4764831986Spetzler RF Martin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:476–483 1986

  • 21.

    Tomlinson FHHouser OWScheithauer BWSundt TM JrOkazaki HParisi JE: Angiographically occult vascular malformations: a correlative study of features on magnetic resonance imaging and histological examination. Neurosurgery 34:7927991994Tomlinson FH Houser OW Scheithauer BW Sundt TM Jr Okazaki H Parisi JE: Angiographically occult vascular malformations: a correlative study of features on magnetic resonance imaging and histological examination. Neurosurgery 34:792–799 1994

  • 22.

    Yamamoto MIde MJimbo MTakakura KLindquist CSteiner L: Neuroimaging studies of postobliteration nidus changes in cerebral arteriovenous malformations treated by gamma knife radiosurgery. Surg Neurol 45:1101221996Yamamoto M Ide M Jimbo M Takakura K Lindquist C Steiner L: Neuroimaging studies of postobliteration nidus changes in cerebral arteriovenous malformations treated by gamma knife radiosurgery. Surg Neurol 45:110–122 1996

  • 23.

    Yamamoto MJimbo MKobayashi MToyoda CIde MTanaka Net al: Long-term results of radiosurgery for arteriovenous malformation: neurodiagnostic imaging and histological studies of angiographically confirmed nidus obliteration. Surg Neurol 37:2192301992Yamamoto M Jimbo M Kobayashi M Toyoda C Ide M Tanaka N et al: Long-term results of radiosurgery for arteriovenous malformation: neurodiagnostic imaging and histological studies of angiographically confirmed nidus obliteration. Surg Neurol 37:219–230 1992

TrendMD

Cited By

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 206 206 65
Full Text Views 100 100 0
PDF Downloads 53 53 0
EPUB Downloads 0 0 0

PubMed

Google Scholar