Histopathological changes in brain arteriovenous malformations after embolization using Onyx or N-butyl cyanoacrylate

Laboratory investigation

View More View Less
  • 1 Departments of Neurological Surgery,
  • 2 Neuroradiology, and
  • 3 Neuropathology, University of Washington, Seattle, Washington
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

The aim of this study was to analyze the histopathological changes in a consecutive series of 32 patients with brain arteriovenous malformations that were resected after undergoing endovascular embolization (22 using Onyx and 10 using N-butyl cyanoacrylate [NBCA]).

Methods

Selections from fixed paraffin-embedded specimens were stained for histological examination with H & E and Verhoeff-van Gieson stain. Lipid dye Oil Red O was used to stain vessel specimens that were embolized using NBCA. Specimens were evaluated for the presence of embolic agent, inflammation, angionecrosis, and evidence of recanalization. These results were correlated with the time interval between the bleeding, embolization, and resection.

Results

The smallest vessel occluded by the embolic agent was 5 μm in the Onyx group and 20 μm in the NBCA group. There was evidence of vascular or perivascular inflammation in 20 (90.9%) of 22 and 9 (90%) of 10 specimens after Onyx and NBCA embolization, respectively. Chronic foreign-body giant cells were observed in 12 (54.5%) of 22 specimens after Onyx embolization, but were absent in specimens after NBCA embolization. Angionecrosis of the embolized vessel was observed in 13 (59.1%) of 22 specimens and in 4 (40%) of 10 specimens after Onyx and NBCA embolization, respectively. There was evidence of recanalization in Onyx embolized vessels in 4 (18.2%) of 22 specimens, and there was no evidence of recanalization after NBCA embolization.

Conclusions

Onyx penetrates much smaller vessels than NBCA. Inflammation occurs with both embolic agents at equal frequency. Evidence of chronic foreign-body giant cells and recanalization after Onyx embolization shows a long-standing reaction to Onyx and raises questions about the permanence of occlusion after Onyx embolization.

Abbreviations used in this paper: AVM = arteriovenous malformation; DMSO = dimethyl sulfoxide; FBGC = foreign-body giant cell; NBCA = N-butyl cyanoacrylate; RBC = red blood cell; VVG = Verhoeff-van Gieson.

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: Laligam N. Sekhar, M.D., Department of Neurological Surgery, Harborview Medical Center, Box 359766, Seattle, Washington 98104. email: lsekhar@u.washington.edu.
  • 1

    Brothers MF, , Kaufmann JC, , Fox AJ, & Deveikis JP: n-Butyl 2-cyanoacrylate—substitute for IBCA in interventional neuroradiology: histopathologic and polymerization time studies. AJNR Am J Neuroradiol 10:777786, 1989

    • Search Google Scholar
    • Export Citation
  • 2

    Carlson AP, , Taylor CL, & Yonas H: Treatment of dural arteriovenous fistula using ethylene vinyl alcohol (onyx) arterial embolization as the primary modality: short-term results. J Neurosurg 107:11201125, 2007

    • Search Google Scholar
    • Export Citation
  • 3

    Cekirge HS, , Saatci I, , Ozturk MH, , Cil B, , Arat A, & Mawad M, : Late angiographic and clinical follow-up results of 100 consecutive aneurysms treated with Onyx reconstruction: largest single-center experience. Neuroradiology 48:113126, 2006

    • Search Google Scholar
    • Export Citation
  • 4

    Chaloupka JC, , Vinuela F, , Vinters HV, & Robert J: Technical feasibility and histopathologic studies of ethylene vinyl copolymer (EVAL) using a swine endovascular embolization model. AJNR Am J Neuroradiol 15:11071115, 1994

    • Search Google Scholar
    • Export Citation
  • 5

    Debrun GM, , Aletich V, , Ausman JI, , Charbel F, & Dujovny M: Embolization of the nidus of brain arteriovenous malformations with n-butyl cyanoacrylate. Neurosurgery 40:112121, 1997

    • Search Google Scholar
    • Export Citation
  • 6

    Deveikis JP: Endovascular therapy of intracranial arteriovenous malformations. Materials and techniques. Neuroimaging Clin N Am 8:401424, 1998

    • Search Google Scholar
    • Export Citation
  • 7

    Duffner F, , Ritz R, , Bornemann A, , Freudenstein D, , Wiendl H, & Siekmann R: Combined therapy of cerebral arteriovenous malformations: histological differences between a non-adhesive liquid embolic agent and n-butyl 2-cyanoacrylate (NBCA). Clin Neuropathol 21:1317, 2002

    • Search Google Scholar
    • Export Citation
  • 8

    Fournier D, , TerBrugge KG, , Willinsky R, , Lasjaunias P, & Montanera W: Endovascular treatment of intracerebral arteriovenous malformations: experience in 49 cases. J Neurosurg 75:228233, 1991

    • Search Google Scholar
    • Export Citation
  • 9

    Fukushima T, , Ohshiro S, , Tsuchimochi H, , Tsugu H, , Tomonaga M, & Gotoh K, : [Clinicopathological evaluation of EVAL embolization in arteriovenous malformations.]. No Shinkei Geka 20:439444, 1992. (Jpn)

    • Search Google Scholar
    • Export Citation
  • 10

    Gobin YP, , Laurent A, , Merienne L, , Schlienger M, , Aymard A, & Houdart E, : Treatment of brain arteriovenous malformations by embolization and radiosurgery. J Neurosurg 85:1928, 1996

    • Search Google Scholar
    • Export Citation
  • 11

    Gruber A, , Mazal PR, , Bavinzski G, , Killer M, , Budka H, & Richling B: Repermeation of partially embolized cerebral arteriovenous malformations: a clinical, radiologic, and histologic study. AJNR Am J Neuroradiol 17:13231331, 1996

    • Search Google Scholar
    • Export Citation
  • 12

    Gruber A, , Ungersbock K, , Reinprecht A, , Czech T, , Gross C, & Bednar M, : Evaluation of cerebral vasospasm after early surgical and endovascular treatment of ruptured intracranial aneurysms. Neurosurgery 42:258268, 1998

    • Search Google Scholar
    • Export Citation
  • 13

    Hamada J, , Kai Y, , Morioka M, , Kazekawa K, , Ishimaru Y, & Iwata H, : A mixture of ethylene vinyl alcohol copolymer and ethanol yielding a nonadhesive liquid embolic agent to treat cerebral arteriovenous malformations: initial clinical experience. J Neurosurg 97:881888, 2002

    • Search Google Scholar
    • Export Citation
  • 14

    Henkes H, , Nahser HC, , Berg-Dammer E, , Weber W, , Lange S, & Kuhne D: Endovascular therapy of brain AVMs prior to radiosurgery. Neurol Res 20:479492, 1998

    • Search Google Scholar
    • Export Citation
  • 15

    Jahan R, , Murayama Y, , Gobin YP, , Duckwiler GR, , Vinters HV, & Vinuela F: Embolization of arteriovenous malformations with Onyx: clinicopathological experience in 23 patients. Neurosurgery 48:984987, 2001

    • Search Google Scholar
    • Export Citation
  • 16

    Lucas Cde P, , Mounayer C, , Spelle L, , Piotin M, , Rezende MT, & Moret J: Endoarterial management of dural arteriovenous malformations with isolated sinus using Onyx-18: technical case report. Neurosurgery 61:2 Suppl E293E294, 2007

    • Search Google Scholar
    • Export Citation
  • 17

    Lundqvist C, , Wikholm G, & Svendsen P: Embolization of cerebral arteriovenous malformations: Part II—Aspects of complications and late outcome. Neurosurgery 39:460469, 1996

    • Search Google Scholar
    • Export Citation
  • 18

    Lv X, , Li Y, & Wu Z: Endovascular treatment of anterior cranial fossa dural arteriovenous fistula. Neuroradiology 50:433 437, 2008

  • 19

    Lylyk P, , Vinuela F, , Vinters HV, , Dion J, , Bentson J, & Duckwiler G, : Use of a new mixture for embolization of intracranial vascular malformations. Preliminary experimental experience. Neuroradiology 32:304310, 1990

    • Search Google Scholar
    • Export Citation
  • 20

    Martin NA, , Khanna R, , Doberstein C, & Bentson J: Therapeutic embolization of arteriovenous malformations: the case for and against. Clin Neurosurg 46:295318, 2000

    • Search Google Scholar
    • Export Citation
  • 21

    Mazal PR, , Stichenwirth M, , Gruber A, , Sulzbacher I, & Hainfellner JA: Tissue reactions induced by different embolising agents in cerebral arteriovenous malformations: a histopathological follow-up. Pathology 38:2832, 2006

    • Search Google Scholar
    • Export Citation
  • 22

    Molyneux AJ, , Cekirge S, , Saatci I, & Gal G: Cerebral Aneurysm Multicenter European Onyx (CAMEO) trial: results of a prospective observational study in 20 European centers. AJNR Am J Neuroradiol 25:3951, 2004

    • Search Google Scholar
    • Export Citation
  • 23

    Mounayer C, , Hammami N, , Piotin M, , Spelle L, , Benndorf G, & Kessler I, : Nidal embolization of brain arteriovenous malformations using Onyx in 94 patients. AJNR Am J Neuroradiol 28:518523, 2007

    • Search Google Scholar
    • Export Citation
  • 24

    Murayama Y, , Malisch T, , Guglielmi G, , Mawad ME, , Vinuela F, & Duckwiler GR, : Incidence of cerebral vasospasm after endovascular treatment of acutely ruptured aneurysms: report on 69 cases. J Neurosurg 87:830835, 1997

    • Search Google Scholar
    • Export Citation
  • 25

    Murayama Y, , Vinuela F, , Ulhoa A, , Akiba Y, , Duckwiler GR, & Gobin YP, : Nonadhesive liquid embolic agent for cerebral arteriovenous malformations: preliminary histopathological studies in swine rete mirabile. Neurosurgery 43:11641175, 1998

    • Search Google Scholar
    • Export Citation
  • 26

    Natarajan SK, , Ghodke B, , Britz GW, , Born DE, & Sekhar LN: Multimodality treatment of brain arteriovenous malformations with microsurgery after embolization with onyx: singlecenter experience and technical nuances. Neurosurgery 62:12131226, 2008

    • Search Google Scholar
    • Export Citation
  • 27

    Pelz DM, , Lownie SP, , Fox AJ, & Hutton LC: Symptomatic pulmonary complications from liquid acrylate embolization of brain arteriovenous malformations. AJNR Am J Neuroradiol 16:1926, 1995

    • Search Google Scholar
    • Export Citation
  • 28

    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
  • 29

    Richling B: Homologous controlled-viscosity fibrin for endovascular embolization. Part I. Experimental development of the medium. Acta Neurochir (Wien) 62:159170, 1982

    • Search Google Scholar
    • Export Citation
  • 30

    Richling B, & Killer M: Endovascular management of patients with cerebral arteriovenous malformations. Neurosurg Clin N Am 11:123145, 2000

    • Search Google Scholar
    • Export Citation
  • 31

    Sampei K, , Hashimoto N, , Kazekawa K, , Tsukahara T, , Iwata H, & Takaichi S: Histological changes in brain tissue and vasculature after intracarotid infusion of organic solvents in rats. Neuroradiology 38:291294, 1996

    • Search Google Scholar
    • Export Citation
  • 32

    Schmutz F, , McAuliffe W, , Anderson DM, , Elliott JP, , Eskridge JM, & Winn HR: Embolization of cerebral arteriovenous malformations with silk: histopathologic changes and hemorrhagic complications. AJNR Am J Neuroradiol 18:12331237, 1997

    • Search Google Scholar
    • Export Citation
  • 33

    Shi ZS, , Feng L, , Jiang XB, , Huang Q, , Yang Z, & Huang ZS: Therapeutic embolization of meningiomas with Onyx for delayed surgical resection. Surg Neurol 70:478481, 2008

    • Search Google Scholar
    • Export Citation
  • 34

    Shi ZS, , Ziegler J, , Gonzalez NR, , Feng L, , Tateshima S, & Jahan R, : Transarterial embolization of clival dural arteriovenous fistulae using liquid embolic agents. Neurosurgery 62:408 415, 2008

    • Search Google Scholar
    • Export Citation
  • 35

    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
  • 36

    Tu J, , Stoodley MA, , Morgan MK, & Storer KP: Ultrastructure of perinidal capillaries in cerebral arteriovenous malformations. Neurosurgery 58:961970, 2006

    • Search Google Scholar
    • Export Citation
  • 37

    van Rooij WJ, , Sluzewski M, & Beute GN: Brain AVM embolization with Onyx. AJNR Am J Neuroradiol 28:172178, 2007

  • 38

    Weber W, , Kis B, , Siekmann R, & Kuehne D: Endovascular treatment of intracranial arteriovenous malformations with onyx: technical aspects. AJNR Am J Neuroradiol 28:371377, 2007

    • Search Google Scholar
    • Export Citation
  • 39

    Weber W, , Siekmann R, , Kis B, & Kuehne D: Treatment and follow-up of 22 unruptured wide-necked intracranial aneurysms of the internal carotid artery with Onyx HD 500. AJNR Am J Neuroradiol 26:19091915, 2005

    • Search Google Scholar
    • Export Citation
  • 40

    Wikholm G, , Lundqvist C, & Svendsen P: The Goteborg cohort of embolized cerebral arteriovenous malformations: a 6-year follow-up. Neurosurgery 49:799806, 2001

    • Search Google Scholar
    • Export Citation
  • 41

    Yakes WF, , Krauth L, , Ecklund J, , Swengle R, , Dreisbach JN, & Seibert CE, : Ethanol endovascular management of brain arteriovenous malformations: initial results. Neurosurgery 40:11451154, 1997

    • Search Google Scholar
    • Export Citation
  • 42

    Yeh HS, , Kashiwagi S, , Tew JM Jr, & Berger TS: Surgical management of epilepsy associated with cerebral arteriovenous malformations. J Neurosurg 72:216223, 1990

    • Search Google Scholar
    • Export Citation
  • 43

    Zanetti PH, & Sherman FE: Experimental evaluation of a tissue adhesive as an agent for the treatment of aneurysms and arteriovenous anomalies. J Neurosurg 36:7279, 1972

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 642 251 21
Full Text Views 247 39 5
PDF Downloads 160 20 1
EPUB Downloads 0 0 0