The effect of preoperative embolization and flow dynamics on resection of brain arteriovenous malformations

View More View Less
  • 1 UCSF School of Medicine and Departments of
  • 2 Anesthesia and Perioperative Care,
  • 3 Radiology and Biomedical Imaging, and
  • 4 Biostatistics and Epidemiology, UCSF Medical Center, San Francisco, California; and
  • 5 Department of Neurological Surgery, Barrow Neurological Institute, Phoenix, Arizona
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

 

OBJECTIVE

Preoperative embolization of brain arteriovenous malformations (AVMs) is performed to facilitate resection, although its impact on surgical performance has not been clearly defined. The authors tested for associations between embolization and surgical performance metrics.

METHODS

The authors analyzed AVM cases resected by one neurosurgeon from 2006 to 2017. They tested whether cases with and without embolization differed from one another with respect to patient and AVM characteristics using t-tests for continuous variables and Fisher’s exact tests for categorical variables. They used simple and multivariable regression models to test whether surgical outcomes (blood loss, resection time, surgical clip usage, and modified Rankin Scale [mRS] score) were associated with embolization. Additional regression analyses integrated the peak arterial afferent contrast normalized for the size of the region of interest (Cmax/ROI) into models as an additional predictor.

RESULTS

The authors included 319 patients, of whom 151 (47%) had preoperative embolization. Embolized AVMs tended to be larger (38% with diameter > 3 cm vs 19%, p = 0.001), less likely to have hemorrhaged (48% vs 63%, p = 0.013), or be diffuse (19% vs 29%, p = 0.045). Embolized AVMs were more likely to have both superficial and deep venous drainage and less likely to have exclusively deep drainage (32% vs 17% and 12% vs 23%, respectively; p = 0.002). In multivariable analysis, embolization was not a significant predictor of blood loss or mRS score changes, but did predict longer operating times (+29 minutes, 95% CI 2–56 minutes; p = 0.034) and increased clip usage (OR 2.61, 95% CI 1.45–4.71; p = 0.001). Cmax/ROI was not a significant predictor, although cases with large Cmax/ROI tended to have longer procedure times (+25 minutes per doubling of Cmax/ROI, 95% CI 0–50 minutes; p = 0.051).

CONCLUSIONS

In this series, preoperative embolization was associated with longer median resection times and had no association with intraoperative blood loss or mRS score changes.

ABBREVIATIONS AVM = arteriovenous malformation; Cmax = peak contrast density of the primary feeding artery; Cmax/ROI = Cmax normalized for the size of the ROI (i.e., the diameter of the artery); EVOH = ethylene vinyl alcohol copolymer; mRS = modified Rankin Scale; NBCA = N-butyl 2-cyanoacrylate; PI = proportional increase; PVA = polyvinyl alcohol; ROI = region of interest.

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

Correspondence Grace F. Donzelli: UCSF Medical Center, San Francisco, CA. gracedonzelli@gmail.com.

INCLUDE WHEN CITING Published online May 17, 2019; DOI: 10.3171/2019.2.JNS182743.

Disclosures Dr. Hetts reports being a consultant for Cerenovus and MicroVention Terumo; ownership of Stryker; direct ownership of stock in ThrombX; and a research contract with Siemens.

  • 1

    Alaraj A, Amin-Hanjani S, Shakur SF, Aletich VA, Ivanov A, Carlson AP, : Quantitative assessment of changes in cerebral arteriovenous malformation hemodynamics after embolization. Stroke 46:942947, 2015

    • Search Google Scholar
    • Export Citation
  • 2

    Burkhardt JK, Chen X, Winkler EA, Cooke DL, Kim H, Lawton MT: Delayed venous drainage in ruptured arteriovenous malformations based on quantitative color-coded digital subtraction angiography. World Neurosurg 104:619627, 2017

    • Search Google Scholar
    • Export Citation
  • 3

    Chen X, Cooke DL, Saloner D, Nelson J, Su H, Lawton MT, : Higher flow is present in unruptured arteriovenous malformations with silent intralesional microhemorrhages. Stroke 48:28812884, 2017

    • Search Google Scholar
    • Export Citation
  • 4

    Conger A, Kulwin C, Lawton MT, Cohen-Gadol AA: Diagnosis and evaluation of intracranial arteriovenous malformations. Surg Neurol Int 6:76, 2015

    • Search Google Scholar
    • Export Citation
  • 5

    DeMeritt JS, Pile-Spellman J, Mast H, Moohan N, Lu DC, Young WL, : Outcome analysis of preoperative embolization with N-butyl cyanoacrylate in cerebral arteriovenous malformations. AJNR Am J Neuroradiol 16:18011807, 1995

    • Search Google Scholar
    • Export Citation
  • 6

    Diehl RR, Henkes H, Nahser HC, Kühne D, Berlit P: Blood flow velocity and vasomotor reactivity in patients with arteriovenous malformations. A transcranial Doppler study. Stroke 25:15741580, 1994

    • Search Google Scholar
    • Export Citation
  • 7

    Ding D, Starke RM, Kano H, Lee JYK, Mathieu D, Pierce J, : Stereotactic radiosurgery for Spetzler-Martin Grade III arteriovenous malformations: an international multicenter study. J Neurosurg 126:859871, 2017

    • Search Google Scholar
    • Export Citation
  • 8

    Elsenousi A, Aletich VA, Alaraj A: Neurological outcomes and cure rates of embolization of brain arteriovenous malformations with n-butyl cyanoacrylate or Onyx: a meta-analysis. J Neurointerv Surg 8:265272, 2016

    • Search Google Scholar
    • Export Citation
  • 9

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

    • Search Google Scholar
    • Export Citation
  • 10

    Jafar JJ, Davis AJ, Berenstein A, Choi IS, Kupersmith MJ: The effect of embolization with N-butyl cyanoacrylate prior to surgical resection of cerebral arteriovenous malformations. J Neurosurg 78:6069, 1993

    • Search Google Scholar
    • Export Citation
  • 11

    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
  • 12

    Lee KW, Tsai FY, Chen WL, Liu CK, Kuo CL: Intracranial venous hemodynamics and rupture of cerebral aneurysm. Neuroradiol J 27:703709, 2014

    • Search Google Scholar
    • Export Citation
  • 13

    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
  • 14

    Morgan MK, Davidson AS, Koustais S, Simons M, Ritson EA: The failure of preoperative ethylene-vinyl alcohol copolymer embolization to improve outcomes in arteriovenous malformation management: case series. J Neurosurg 118:969977, 2013

    • Search Google Scholar
    • Export Citation
  • 15

    Morgan MK, Zurin AAR, Harrington T, Little N: Changing role for preoperative embolisation in the management of arteriovenous malformations of the brain. J Clin Neurosci 7:527530, 2000

    • Search Google Scholar
    • Export Citation
  • 16

    n-BCA Trial Investigators: N-butyl cyanoacrylate embolization of cerebral arteriovenous malformations: results of a prospective, randomized, multi-center trial. AJNR Am J Neuroradiol 23:748755, 2002

    • Search Google Scholar
    • Export Citation
  • 17

    Norris JS, Valiante TA, Wallace MC, Willinsky RA, Montanera WJ, terBrugge KG, : A simple relationship between radiological arteriovenous malformation hemodynamics and clinical presentation: a prospective, blinded analysis of 31 cases. J Neurosurg 90:673679, 1999

    • Search Google Scholar
    • Export Citation
  • 18

    Ogilvy CS, Stieg PE, Awad I, Brown RD Jr, Kondziolka D, Rosenwasser R, : 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 32:14581471, 2001

    • Search Google Scholar
    • Export Citation
  • 19

    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
  • 20

    Pasqualin A, Scienza R, Cioffi F, Barone G, Benati A, Beltramello A, : Treatment of cerebral arteriovenous malformations with a combination of preoperative embolization and surgery. Neurosurgery 29:358368, 1991

    • Search Google Scholar
    • Export Citation
  • 21

    Patibandla MR, Ding D, Kano H, Xu Z, Lee JYK, Mathieu D, : Stereotactic radiosurgery for Spetzler-Martin Grade IV and V arteriovenous malformations: an international multicenter study. J Neurosurg 129:498507, 2018

    • Search Google Scholar
    • Export Citation
  • 22

    Purdy PD, Samson D, Batjer HH, Risser RC: Preoperative embolization of cerebral arteriovenous malformations with polyvinyl alcohol particles: experience in 51 adults. AJNR Am J Neuroradiol 11:501510, 1990

    • Search Google Scholar
    • Export Citation
  • 23

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

  • 24

    Spetzler RF, Martin NA, Carter LP, Flom RA, Raudzens PA, Wilkinson E: Surgical management of large AVM’s by staged embolization and operative excision. J Neurosurg 67:1728, 1987

    • Search Google Scholar
    • Export Citation
  • 25

    Starke RM, Komotar RJ, Otten ML, Hahn DK, Fischer LE, Hwang BY, : Adjuvant embolization with N-butyl cyanoacrylate in the treatment of cerebral arteriovenous malformations: outcomes, complications, and predictors of neurologic deficits. Stroke 40:27832790, 2009

    • Search Google Scholar
    • Export Citation
  • 26

    Todaka T, Hamada J, Kai Y, Morioka M, Ushio Y: Analysis of mean transit time of contrast medium in ruptured and unruptured arteriovenous malformations: a digital subtraction angiographic study. Stroke 34:24102414, 2003

    • Search Google Scholar
    • Export Citation
  • 27

    van Beijnum J, van der Worp HB, Buis DR, Al-Shahi Salman R, Kappelle LJ, Rinkel GJE, : Treatment of brain arteriovenous malformations: a systematic review and meta-analysis. JAMA 306:20112019, 2011

    • Search Google Scholar
    • Export Citation
  • 28

    van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J: Interobserver agreement for the assessment of handicap in stroke patients. Stroke 19:604607, 1988

    • Search Google Scholar
    • Export Citation
  • 29

    Viñuela F, Dion JE, Duckwiler G, Martin NA, Lylyk P, Fox A, : Combined endovascular embolization and surgery in the management of cerebral arteriovenous malformations: experience with 101 cases. J Neurosurg 75:856864, 1991

    • Search Google Scholar
    • Export Citation
  • 30

    Weber W, Kis B, Siekmann R, Jans P, Laumer R, Kühne D: Preoperative embolization of intracranial arteriovenous malformations with Onyx. Neurosurgery 61:244254, 2007

    • Search Google Scholar
    • Export Citation
  • 31

    Wong J, Slomovic A, Ibrahim G, Radovanovic I, Tymianski M: Microsurgery for ARUBA Trial (A Randomized Trial of Unruptured Brain Arteriovenous Malformation)–eligible unruptured brain arteriovenous malformations. Stroke 48:136144, 2017

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 100 100 62
Full Text Views 73 73 51
PDF Downloads 100 100 61
EPUB Downloads 0 0 0