Stereotactic radiosurgery of the rete mirabile in swine: A longitudinal study of histopathological changes

Reza Jahan, Timothy D. Solberg, Daniel Lee, Paul Medin, Satoshi Tateshima, James Sayre, Antonio De Salles, Harry V. Vinters, Fernando Vinuela

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

OBJECTIVE:: Stereotactic radiosurgery is an established, effective treatment for brain arteriovenous malformations. The mechanisms of vessel occlusion in arteriovenous malformations has not been extensively evaluated. To better understand these mechanisms, we report histopathological changes in the swine rete mirabile after stereotactic radiosurgery. METHODS:: Thirty-five swine were used, 15 as nonradiated controls and 20 as radiated. Two in the control group and five in the radiated group were sacrificed before the study endpoint. Tissue was obtained from 13 nonradiated (4 at 3 mo, 5 at 6 mo, 4 at 9 mo) and 15 radiated swine (2 at 3 mo, 3 at 6 mo, 10 at 9 mo) for histological, immunohistochemical, and morphometric analysis. RESULTS:: Radiated vessels showed increasing intimal hyperplasia over the follow-up period. Histometrical analysis confirmed this with evidence of progressive luminal narrowing over the follow-up period. Immunohistochemical analysis showed intimal cells to be proliferating smooth muscle cells with surrounding extracellular collagen Type IV. Adventitial fibrosis composed of collagen Type IV was also seen with smooth muscle cells interspersed within the collagen matrix. The nonradiated animals showed no intimal hyperplasia or change in the appearance or size of the vessels over the same follow-up period. Adventitial fibrosis was minimal in the nonradiated animals. CONCLUSION:: The vessels show an intimal response to radiation with progressive occlusion caused by migrating, proliferating smooth muscle cells, a likely source of the extracellular collagen in the intima. Cytokine mediated pathways likely produce these morphological changes. Future studies will be directed toward elucidating these underlying molecular mechanisms.

Original languageEnglish (US)
Pages (from-to)551-558
Number of pages8
JournalNeurosurgery
Volume58
Issue number3
DOIs
StatePublished - Mar 2006

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Tunica Intima
Radiosurgery
Longitudinal Studies
Swine
Smooth Muscle Myocytes
Adventitia
Collagen Type IV
Arteriovenous Malformations
Hyperplasia
Fibrosis
Collagen Type VI
Collagen
Radiation
Cytokines
Control Groups
Brain

Keywords

  • Animal model
  • Arteriovenous malformation
  • Radiosurgery
  • Swine

ASJC Scopus subject areas

  • Clinical Neurology
  • Surgery

Cite this

Stereotactic radiosurgery of the rete mirabile in swine : A longitudinal study of histopathological changes. / Jahan, Reza; Solberg, Timothy D.; Lee, Daniel; Medin, Paul; Tateshima, Satoshi; Sayre, James; De Salles, Antonio; Vinters, Harry V.; Vinuela, Fernando.

In: Neurosurgery, Vol. 58, No. 3, 03.2006, p. 551-558.

Research output: Contribution to journalArticle

Jahan, R, Solberg, TD, Lee, D, Medin, P, Tateshima, S, Sayre, J, De Salles, A, Vinters, HV & Vinuela, F 2006, 'Stereotactic radiosurgery of the rete mirabile in swine: A longitudinal study of histopathological changes', Neurosurgery, vol. 58, no. 3, pp. 551-558. https://doi.org/10.1227/01.NEU.0000197335.93538.BD
Jahan, Reza ; Solberg, Timothy D. ; Lee, Daniel ; Medin, Paul ; Tateshima, Satoshi ; Sayre, James ; De Salles, Antonio ; Vinters, Harry V. ; Vinuela, Fernando. / Stereotactic radiosurgery of the rete mirabile in swine : A longitudinal study of histopathological changes. In: Neurosurgery. 2006 ; Vol. 58, No. 3. pp. 551-558.
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T2 - A longitudinal study of histopathological changes

AU - Jahan, Reza

AU - Solberg, Timothy D.

AU - Lee, Daniel

AU - Medin, Paul

AU - Tateshima, Satoshi

AU - Sayre, James

AU - De Salles, Antonio

AU - Vinters, Harry V.

AU - Vinuela, Fernando

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N2 - OBJECTIVE:: Stereotactic radiosurgery is an established, effective treatment for brain arteriovenous malformations. The mechanisms of vessel occlusion in arteriovenous malformations has not been extensively evaluated. To better understand these mechanisms, we report histopathological changes in the swine rete mirabile after stereotactic radiosurgery. METHODS:: Thirty-five swine were used, 15 as nonradiated controls and 20 as radiated. Two in the control group and five in the radiated group were sacrificed before the study endpoint. Tissue was obtained from 13 nonradiated (4 at 3 mo, 5 at 6 mo, 4 at 9 mo) and 15 radiated swine (2 at 3 mo, 3 at 6 mo, 10 at 9 mo) for histological, immunohistochemical, and morphometric analysis. RESULTS:: Radiated vessels showed increasing intimal hyperplasia over the follow-up period. Histometrical analysis confirmed this with evidence of progressive luminal narrowing over the follow-up period. Immunohistochemical analysis showed intimal cells to be proliferating smooth muscle cells with surrounding extracellular collagen Type IV. Adventitial fibrosis composed of collagen Type IV was also seen with smooth muscle cells interspersed within the collagen matrix. The nonradiated animals showed no intimal hyperplasia or change in the appearance or size of the vessels over the same follow-up period. Adventitial fibrosis was minimal in the nonradiated animals. CONCLUSION:: The vessels show an intimal response to radiation with progressive occlusion caused by migrating, proliferating smooth muscle cells, a likely source of the extracellular collagen in the intima. Cytokine mediated pathways likely produce these morphological changes. Future studies will be directed toward elucidating these underlying molecular mechanisms.

AB - OBJECTIVE:: Stereotactic radiosurgery is an established, effective treatment for brain arteriovenous malformations. The mechanisms of vessel occlusion in arteriovenous malformations has not been extensively evaluated. To better understand these mechanisms, we report histopathological changes in the swine rete mirabile after stereotactic radiosurgery. METHODS:: Thirty-five swine were used, 15 as nonradiated controls and 20 as radiated. Two in the control group and five in the radiated group were sacrificed before the study endpoint. Tissue was obtained from 13 nonradiated (4 at 3 mo, 5 at 6 mo, 4 at 9 mo) and 15 radiated swine (2 at 3 mo, 3 at 6 mo, 10 at 9 mo) for histological, immunohistochemical, and morphometric analysis. RESULTS:: Radiated vessels showed increasing intimal hyperplasia over the follow-up period. Histometrical analysis confirmed this with evidence of progressive luminal narrowing over the follow-up period. Immunohistochemical analysis showed intimal cells to be proliferating smooth muscle cells with surrounding extracellular collagen Type IV. Adventitial fibrosis composed of collagen Type IV was also seen with smooth muscle cells interspersed within the collagen matrix. The nonradiated animals showed no intimal hyperplasia or change in the appearance or size of the vessels over the same follow-up period. Adventitial fibrosis was minimal in the nonradiated animals. CONCLUSION:: The vessels show an intimal response to radiation with progressive occlusion caused by migrating, proliferating smooth muscle cells, a likely source of the extracellular collagen in the intima. Cytokine mediated pathways likely produce these morphological changes. Future studies will be directed toward elucidating these underlying molecular mechanisms.

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