Experimental radiosurgery simulations using a theoretical model of cerebral arteriovenous malformations

Tarik F. Massoud, George J. Hademenos, Antonio A F De Salles, Timothy D. Solberg

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Background and Purpose - A novel biomathematical arteriovenous malformation (AVM) model based on electric network analysis was used to investigate theoretically the potential role of intranidal hemodynamic perturbations in elevating the risk of rupture after simulated brain AVM radiosurgery. Methods - The effects of radiation on 28 interconnected plexiform and fistulous AVM nidus vessels were simulated by predefined random or stepwise occlusion. Electric circuit analysis revealed the changes in intranidal flow, pressure, and risk of rupture at intervals of 3 months during a 3-year latency period after simulated partial/complete irradiation of the nidus using doses <25 and ≥25 Gy. An expression for risk of rupture was derived on the basis of the functional distribution of the critical radii of component vessels. The theoretical effects of radiation were also tested on AVM nidus vessels with progressively increasing elastic modulus (E) and wall thickness during the latency period, simulating their eventual fibrosis. Results - In an AVM with E=5.0 X 104 dyne/cm2, 4 (14.3%) of a total 28 sets of AVM radiosurgery simulations revealed theoretical nidus rupture (risk of rupture ≥ 100%). Three of these were associated with partial nidus coverage and 1 with complete treatment. All ruptures occurred after random occlusion of nidus vessels in AVMs receiving low-dose radiosurgery. Intranidal hemodynamic perturbations were observed in all cases of AVM rupture; the occlusion of a fistulous component resulted in intranidal rerouting of flow and escalation of the intravascular pressure in adjacent plexiform components. Risk of rupture was found to correlate with nidus vessel wall strength: A low E of 1.9 X 104 dyne/cm2 resulted in a 92.8% incidence of AVM rupture, whereas a higher E of 7.0 X 104 dyne/cm2 resulted in only a 3.6% incidence of AVM rupture. A dramatic reduction in rupture incidence was observed when increasing fibrosis of the nidus was modeled during the latency period. Conclusions - It was found that the theoretical occurrence of AVM hemorrhage after radiosurgery was low, particularly when radiation-induced fibrosis of nidus vessels was considered. When rupture does occur, it would appear from a theoretical standpoint that the occlusion of intranidal fistulas or larger-caliber plexiform vessels could be a significant culprit in the generation of critical intranidal hemodynamic surges resulting in nidus rupture. The described AVM model should serve as a useful research tool for further theoretical investigations of cerebral AVM radiosurgery and its hemodynamic sequelae.

Original languageEnglish (US)
Pages (from-to)2466-2477
Number of pages12
JournalStroke
Volume31
Issue number10
StatePublished - 2000

Fingerprint

Intracranial Arteriovenous Malformations
Radiosurgery
Arteriovenous Malformations
Rupture
Theoretical Models
Hemodynamics
Radiation Effects
Incidence
Fibrosis
Radiation Pneumonitis
Pressure
Elastic Modulus
Fistula

Keywords

  • Cerebral arteriovenous malformations
  • Hemodynamics
  • Intracerebral hemorrhage
  • Models, theoretical
  • Radiosurgery

ASJC Scopus subject areas

  • Cardiology and Cardiovascular Medicine
  • Neuroscience(all)

Cite this

Massoud, T. F., Hademenos, G. J., De Salles, A. A. F., & Solberg, T. D. (2000). Experimental radiosurgery simulations using a theoretical model of cerebral arteriovenous malformations. Stroke, 31(10), 2466-2477.

Experimental radiosurgery simulations using a theoretical model of cerebral arteriovenous malformations. / Massoud, Tarik F.; Hademenos, George J.; De Salles, Antonio A F; Solberg, Timothy D.

In: Stroke, Vol. 31, No. 10, 2000, p. 2466-2477.

Research output: Contribution to journalArticle

Massoud, TF, Hademenos, GJ, De Salles, AAF & Solberg, TD 2000, 'Experimental radiosurgery simulations using a theoretical model of cerebral arteriovenous malformations', Stroke, vol. 31, no. 10, pp. 2466-2477.
Massoud TF, Hademenos GJ, De Salles AAF, Solberg TD. Experimental radiosurgery simulations using a theoretical model of cerebral arteriovenous malformations. Stroke. 2000;31(10):2466-2477.
Massoud, Tarik F. ; Hademenos, George J. ; De Salles, Antonio A F ; Solberg, Timothy D. / Experimental radiosurgery simulations using a theoretical model of cerebral arteriovenous malformations. In: Stroke. 2000 ; Vol. 31, No. 10. pp. 2466-2477.
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abstract = "Background and Purpose - A novel biomathematical arteriovenous malformation (AVM) model based on electric network analysis was used to investigate theoretically the potential role of intranidal hemodynamic perturbations in elevating the risk of rupture after simulated brain AVM radiosurgery. Methods - The effects of radiation on 28 interconnected plexiform and fistulous AVM nidus vessels were simulated by predefined random or stepwise occlusion. Electric circuit analysis revealed the changes in intranidal flow, pressure, and risk of rupture at intervals of 3 months during a 3-year latency period after simulated partial/complete irradiation of the nidus using doses <25 and ≥25 Gy. An expression for risk of rupture was derived on the basis of the functional distribution of the critical radii of component vessels. The theoretical effects of radiation were also tested on AVM nidus vessels with progressively increasing elastic modulus (E) and wall thickness during the latency period, simulating their eventual fibrosis. Results - In an AVM with E=5.0 X 104 dyne/cm2, 4 (14.3{\%}) of a total 28 sets of AVM radiosurgery simulations revealed theoretical nidus rupture (risk of rupture ≥ 100{\%}). Three of these were associated with partial nidus coverage and 1 with complete treatment. All ruptures occurred after random occlusion of nidus vessels in AVMs receiving low-dose radiosurgery. Intranidal hemodynamic perturbations were observed in all cases of AVM rupture; the occlusion of a fistulous component resulted in intranidal rerouting of flow and escalation of the intravascular pressure in adjacent plexiform components. Risk of rupture was found to correlate with nidus vessel wall strength: A low E of 1.9 X 104 dyne/cm2 resulted in a 92.8{\%} incidence of AVM rupture, whereas a higher E of 7.0 X 104 dyne/cm2 resulted in only a 3.6{\%} incidence of AVM rupture. A dramatic reduction in rupture incidence was observed when increasing fibrosis of the nidus was modeled during the latency period. Conclusions - It was found that the theoretical occurrence of AVM hemorrhage after radiosurgery was low, particularly when radiation-induced fibrosis of nidus vessels was considered. When rupture does occur, it would appear from a theoretical standpoint that the occlusion of intranidal fistulas or larger-caliber plexiform vessels could be a significant culprit in the generation of critical intranidal hemodynamic surges resulting in nidus rupture. The described AVM model should serve as a useful research tool for further theoretical investigations of cerebral AVM radiosurgery and its hemodynamic sequelae.",
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AU - Hademenos, George J.

AU - De Salles, Antonio A F

AU - Solberg, Timothy D.

PY - 2000

Y1 - 2000

N2 - Background and Purpose - A novel biomathematical arteriovenous malformation (AVM) model based on electric network analysis was used to investigate theoretically the potential role of intranidal hemodynamic perturbations in elevating the risk of rupture after simulated brain AVM radiosurgery. Methods - The effects of radiation on 28 interconnected plexiform and fistulous AVM nidus vessels were simulated by predefined random or stepwise occlusion. Electric circuit analysis revealed the changes in intranidal flow, pressure, and risk of rupture at intervals of 3 months during a 3-year latency period after simulated partial/complete irradiation of the nidus using doses <25 and ≥25 Gy. An expression for risk of rupture was derived on the basis of the functional distribution of the critical radii of component vessels. The theoretical effects of radiation were also tested on AVM nidus vessels with progressively increasing elastic modulus (E) and wall thickness during the latency period, simulating their eventual fibrosis. Results - In an AVM with E=5.0 X 104 dyne/cm2, 4 (14.3%) of a total 28 sets of AVM radiosurgery simulations revealed theoretical nidus rupture (risk of rupture ≥ 100%). Three of these were associated with partial nidus coverage and 1 with complete treatment. All ruptures occurred after random occlusion of nidus vessels in AVMs receiving low-dose radiosurgery. Intranidal hemodynamic perturbations were observed in all cases of AVM rupture; the occlusion of a fistulous component resulted in intranidal rerouting of flow and escalation of the intravascular pressure in adjacent plexiform components. Risk of rupture was found to correlate with nidus vessel wall strength: A low E of 1.9 X 104 dyne/cm2 resulted in a 92.8% incidence of AVM rupture, whereas a higher E of 7.0 X 104 dyne/cm2 resulted in only a 3.6% incidence of AVM rupture. A dramatic reduction in rupture incidence was observed when increasing fibrosis of the nidus was modeled during the latency period. Conclusions - It was found that the theoretical occurrence of AVM hemorrhage after radiosurgery was low, particularly when radiation-induced fibrosis of nidus vessels was considered. When rupture does occur, it would appear from a theoretical standpoint that the occlusion of intranidal fistulas or larger-caliber plexiform vessels could be a significant culprit in the generation of critical intranidal hemodynamic surges resulting in nidus rupture. The described AVM model should serve as a useful research tool for further theoretical investigations of cerebral AVM radiosurgery and its hemodynamic sequelae.

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KW - Hemodynamics

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