Multimodality management of Spetzler-Martin Grade III arteriovenous malformations

Clinical article

Paritosh Pandey M.D.1,3, Michael P. Marks M.D.1,2,3, Ciara D. Harraher M.D., M.P.H.1,3, Erick M. Westbroek B.S.1,3, Steven D. Chang M.D.1,3, Huy M. Do M.D.1,2,3, Richard P. Levy M.D., Ph.D.4, Robert L. Dodd M.D., Ph.D.1,2,3, and Gary K. Steinberg M.D., Ph.D.1,3
View More View Less
  • 1 Departments of Neurosurgery and
  • | 2 Radiology,
  • | 3 Stanford Stroke Center and Stanford Institute for Neuro-Innovation and Translational Neurosciences, Stanford University School of Medicine, Stanford, California; and
  • | 4 Department of Radiation Oncology, Loma Linda Medical Center, Loma Linda, California
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

Object

Grade III arteriovenous malformations (AVMs) are diverse because of their variations in size (S), location in eloquent cortex (E), and presence of central venous drainage (V). Because they may have implications for management and outcome, the authors evaluated these variations in the present study.

Methods

Between 1984 and 2010, 100 patients with Grade III AVMs were treated. The AVMs were categorized by Spetzler-Martin characteristics as follows: Type 1 = S1E1V1, Type 2 = S2E1V0, Type 3 = S2E0V1, and Type 4 = S3E0V0. The occurrence of a new neurological deficit, functional status (based on modified Rankin Scale [mRS] score) at discharge and follow-up, and radiological obliteration were correlated with demographic and morphological characteristics.

Results

One hundred patients (49 female and 51 male; age range 5–68 years, mean 35.8 years) were evaluated. The size of AVMs was less than 3 cm in 28 patients, 3–6 cm in 71, and greater than 6 cm in 1; 86 AVMs were located in eloquent cortex and 38 had central drainage. The AVMs were Type 1 in 28 cases, Type 2 in 60, Type 3 in 11, and Type 4 in 1. The authors performed embolization in 77 patients (175 procedures), surgery in 64 patients (74 surgeries), and radiosurgery in 49 patients (44 primary and 5 postoperative).

The mortality rate following the management of these AVMs was 1%. Fourteen patients (14%) had new neurological deficits, with 5 (5%) being disabling (mRS score > 2) and 9 (9%) being nondisabling (mRS score ≤ 2) events. Patients with Type 1 AVMs (small size) had the best outcome, with 1 (3.6%) in 28 having a new neurological deficit, compared with 72 patients with larger AVMs, of whom 13 (18.1%) had a new neurological deficit (p < 0.002). Older age (> 40 years), malformation size > 3 cm, and nonhemorrhagic presentation predicted the occurrence of new deficits (p < 0.002). Sex, eloquent cortex, and venous drainage did not confer any benefit.

In 89 cases follow-up was adequate for data to be included in the obliteration analysis. The AVM was obliterated in 78 patients (87.6%), 69 of them (88.5%) demonstrated on angiography and 9 on MRI /MR angiography. There was no difference between obliteration rates between different types of AVMs, size, eloquence, and drainage. Age, sex, and clinical presentation also did not predict obliteration.

Conclusions

Multimodality management of Grade III AVMs results in a high rate of obliteration, which was not influenced by size, venous drainage, or eloquent location. However, the development of new neurological deficits did correlate with size, whereas eloquence and venous drainage did not affect the neurological complication rate. The authors propose subclassifying the Grade III AVMs according to their size (< 3 and ≥ 3 cm) to account for treatment risk.

Abbreviations used in this paper:

AVM = arteriovenous malformation; MRA = MR angiography; mRS = modified Rankin Scale.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Address correspondence to: Gary K. Steinberg, M.D., Ph.D., R281, Department of Neurosurgery, Stanford University School of Medicine, 300 Pasteur Drive, Stanford, California 94305-5327. email: gsteinberg@stanford.edu.

Please include this information when citing this paper: published online April 6, 2012; DOI: 10.3171/2012.3.JNS111575.

  • 1

    Andrade-Souza YM, , Zadeh G, , Ramani M, , Scora D, , Tsao MN, & Schwartz ML: Testing the radiosurgery-based arteriovenous malformation score and the modified Spetzler-Martin grading system to predict radiosurgical outcome. J Neurosurg 103:642648, 2005

    • Search Google Scholar
    • Export Citation
  • 2

    Chang SD, , Marcellus ML, , Marks MP, , Levy RP, , Do HM, & Steinberg GK: Multimodality treatment of giant intracranial arteriovenous malformations. Neurosurgery 53:113, 2003

    • Search Google Scholar
    • Export Citation
  • 3

    Davidson AS, & Morgan MK: How safe is arteriovenous malformation surgery? A prospective, observational study of surgery as first-line treatment for brain arteriovenous malformations. Neurosurgery 66:498505, 2010

    • Search Google Scholar
    • Export Citation
  • 4

    de Oliveira E, , Tedeschi H, & Raso J: Comprehensive management of arteriovenous malformations. Neurol Res 20:673683, 1998

  • 5

    Deruty R, , Pelissou-Guyotat I, , Mottolese C, , Amat D, & Bascoulergue Y: Prognostic value of the Spetzler's grading system in a series of cerebral AVMs treated by a combined management. Acta Neurochir (Wien) 131:169175, 1994

    • Search Google Scholar
    • Export Citation
  • 6

    Du R, , Keyoung HM, , Dowd CF, , Young WL, & Lawton MT: The effects of diffuseness and deep perforating artery supply on outcomes after microsurgical resection of brain arteriovenous malformations. Neurosurgery 60:638648, 2007

    • Search Google Scholar
    • Export Citation
  • 7

    Ferch RD, & Morgan MK: High-grade arteriovenous malformations and their management. J Clin Neurosci 9:3740, 2002

  • 8

    Friedman WA, , Bova FJ, , Bollampally S, & Bradshaw P: Analysis of factors predictive of success or complications in arteriovenous malformation radiosurgery. Neurosurgery 52:296308, 2003

    • Search Google Scholar
    • Export Citation
  • 9

    Hamilton MG, & Spetzler RF: The prospective application of a grading system for arteriovenous malformations. Neurosurgery 34:27, 1994

  • 10

    Han PP, , Ponce FA, & Spetzler RF: Intention-to-treat analysis of Spetzler-Martin grades IV and V arteriovenous malformations: natural history and treatment paradigm. J Neurosurg 98:37, 2003

    • Search Google Scholar
    • Export Citation
  • 11

    Hartmann A, , Mast H, , Mohr JP, , Pile-Spellman J, , Connolly ES, & Sciacca RR, et al. : Determinants of staged endovascular and surgical treatment outcome of brain arteriovenous malformations. Stroke 36:24312435, 2005

    • Search Google Scholar
    • Export Citation
  • 12

    Hartmann A, , Pile-Spellman J, , Stapf C, , Sciacca RR, , Faulstich A, & Mohr JP, et al. : Risk of endovascular treatment of brain arteriovenous malformations. Stroke 33:18161820, 2002

    • Search Google Scholar
    • Export Citation
  • 13

    Hartmann A, , Stapf C, , Hofmeister C, , Mohr JP, , Sciacca RR, & Stein BM, et al. : Determinants of neurological outcome after surgery for brain arteriovenous malformation. Stroke 31:23612364, 2000

    • Search Google Scholar
    • Export Citation
  • 14

    Heros RC, , Korosue K, & Diebold PM: Surgical excision of cerebral arteriovenous malformations: late results. Neurosurgery 26:570578, 1990

    • Search Google Scholar
    • Export Citation
  • 15

    Jayaraman MV, , Marcellus ML, , Do HM, , Chang SD, , Rosenberg JK, & Steinberg GK, et al. : Hemorrhage rate in patients with Spetzler-Martin grades IV and V arteriovenous malformations: is treatment justified?. Stroke 38:325329, 2007

    • Search Google Scholar
    • Export Citation
  • 16

    Kelly ME, , Guzman R, , Sinclair J, , Bell-Stephens TE, , Bower R, & Hamilton S, et al. : Multimodality treatment of posterior fossa arteriovenous malformations. J Neurosurg 108:11521161, 2008

    • Search Google Scholar
    • Export Citation
  • 17

    Kiriş T, , Sencer A, , Sahinbaş M, , Sencer S, , Imer M, & Izgi N: Surgical results in pediatric Spetzler-Martin grades I–III intracranial arteriovenous malformations. Childs Nerv Syst 21:6976, 2005

    • Search Google Scholar
    • Export Citation
  • 18

    Lawton MT: Spetzler-Martin Grade III arteriovenous malformations: surgical results and a modification of the grading scale. Neurosurgery 52:740749, 2003

    • Search Google Scholar
    • Export Citation
  • 19

    Lawton MT, , Du R, , Tran MN, , Achrol AS, , McCulloch CE, & Johnston SC, et al. : Effect of presenting hemorrhage on outcome after microsurgical resection of brain arteriovenous malformations. Neurosurgery 56:485493, 2005

    • Search Google Scholar
    • Export Citation
  • 20

    Lawton MT, , Kim H, , McCulloch CE, , Mikhak B, & Young WL: A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery 66:702713, 2010

    • Search Google Scholar
    • Export Citation
  • 21

    Loh Y, & Duckwiler GR: A prospective, multicenter, randomized trial of the Onyx liquid embolic system and N-butyl cyanoacrylate embolization of cerebral arteriovenous malformations. Clinical article. J Neurosurg 113:733741, 2010

    • Search Google Scholar
    • Export Citation
  • 22

    Luessenhop AJ, & Gennarelli TA: Anatomical grading of supratentorial arteriovenous malformations for determining operability. Neurosurgery 1:3035, 1977

    • Search Google Scholar
    • Export Citation
  • 23

    Morgan MK, , Drummond KJ, , Grinnell V, & Sorby W: Surgery for cerebral arteriovenous malformation: risks related to lenticulostriate arterial supply. J Neurosurg 86:801805, 1997

    • Search Google Scholar
    • Export Citation
  • 24

    Morgan MK, , Rochford AM, , Tsahtsarlis A, , Little N, & Faulder KC: Surgical risks associated with the management of Grade I and II brain arteriovenous malformations. Neurosurgery 61:1 Suppl 417424, 2007

    • Search Google Scholar
    • Export Citation
  • 25

    Pasqualin A, , Barone G, , Cioffi F, , Rosta L, , Scienza R, & Da Pian R: The relevance of anatomic and hemodynamic factors to a classification of cerebral arteriovenous malformations. Neurosurgery 28:370379, 1991

    • Search Google Scholar
    • Export Citation
  • 26

    Paulsen RD, , Steinberg GK, , Norbash AM, , Marcellus ML, , Lopez JR, & Marks MP: Embolization of rolandic cortex arteriovenous malformations. Neurosurgery 44:479486, 1999

    • Search Google Scholar
    • Export Citation
  • 27

    Pellettieri L, , Carlsson CA, , Grevsten S, , Norlén G, & Uhlemann C: Surgical versus conservative treatment of intracranial arteriovenous malformations: a study in surgical decision-making. Acta Neurochir Suppl (Wien) 29:186, 1979

    • Search Google Scholar
    • Export Citation
  • 28

    Pertuiset B, , Ancri D, , Kinuta Y, , Haisa T, , Bordi L, & Lin C, et al. : Classification of supratentorial arteriovenous malformations. A score system for evaluation of operability and surgical strategy based on an analysis of 66 cases. Acta Neurochir (Wien) 110:616, 1991

    • Search Google Scholar
    • Export Citation
  • 29

    Pollock BE, & Flickinger JC: Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery 63:239243, 2008

    • Search Google Scholar
    • Export Citation
  • 30

    Pollock BE, & Flickinger JC: A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg 96:7985, 2002

  • 31

    Pollock BE, , Lunsford LD, , Kondziolka D, , Maitz A, & Flickinger JC: Patient outcomes after stereotactic radiosurgery for “operable” arteriovenous malformations. Neurosurgery 35:18, 1994

    • Search Google Scholar
    • Export Citation
  • 32

    Shi YQ, & Chen XC: A proposed scheme for grading intracranial arteriovenous malformations. J Neurosurg 65:484489, 1986

  • 33

    Spears J, , Terbrugge KG, , Moosavian M, , Montanera W, , Willinsky RA, & Wallace MC, et al. : A discriminative prediction model of neurological outcome for patients undergoing surgery of brain arteriovenous malformations. Stroke 37:14571464, 2006

    • Search Google Scholar
    • Export Citation
  • 34

    Spetzler RF, & Martin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:476483, 1986

  • 35

    Spetzler RF, & Ponce FA: A 3-tier classification of cerebral arteriovenous malformations. Clinical article. J Neurosurg 114:842849, 2011

    • Search Google Scholar
    • Export Citation
  • 36

    Wedderburn CJ, , van Beijnum J, , Bhattacharya JJ, , Counsell CE, , Papanastassiou V, & Ritchie V, et al. : Outcome after interventional or conservative management of unruptured brain arteriovenous malformations: a prospective, population-based cohort study. Lancet Neurol 7:223230, 2008

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 1036 278 27
Full Text Views 233 24 0
PDF Downloads 179 10 0
EPUB Downloads 0 0 0