Vascular compactness of unruptured brain arteriovenous malformation predicts risk of hemorrhage after stereotactic radiosurgery

Po Wei Huang; Syu Jyun Peng; David Hung Chi Pan; Huai Che Yang; Jo Ting Tsai; Cheng Ying Shiau; I. Chang Su; Ching Jen Chen; Hsiu Mei Wu; Chung Jung Lin; Wen Yuh Chung; Wan Yuo Guo; Wei Lun Lo; Shao Wen Lai; Cheng Chia Lee

doi:10.1038/s41598-024-54369-2

Vascular compactness of unruptured brain arteriovenous malformation predicts risk of hemorrhage after stereotactic radiosurgery

Po Wei Huang, Syu Jyun Peng, David Hung Chi Pan, Huai Che Yang, Jo Ting Tsai, Cheng Ying Shiau, I. Chang Su, Ching Jen Chen, Hsiu Mei Wu, Chung Jung Lin, Wen Yuh Chung, Wan Yuo Guo, Wei Lun Lo, Shao Wen Lai, Cheng Chia Lee

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Abstract

The aim of the study was to investigate whether morphology (i.e. compact/diffuse) of brain arteriovenous malformations (bAVMs) correlates with the incidence of hemorrhagic events in patients receiving Stereotactic Radiosurgery (SRS) for unruptured bAVMs. This retrospective study included 262 adult patients with unruptured bAVMs who underwent upfront SRS. Hemorrhagic events were defined as evidence of blood on CT or MRI. The morphology of bAVMs was evaluated using automated segmentation which calculated the proportion of vessel, brain tissue, and cerebrospinal fluid in bAVMs on T2-weighted MRI. Compactness index, defined as the ratio of vessel to brain tissue, categorized bAVMs into compact and diffuse types based on the optimal cutoff. Cox proportional hazard model was used to identify the independent factors for post-SRS hemorrhage. The median clinical follow-ups was 62.1 months. Post-SRS hemorrhage occurred in 13 (5.0%) patients and one of them had two bleeds, resulting in an annual bleeding rate of 0.8%. Multivariable analysis revealed bAVM morphology (compact versus diffuse), bAVM volume, and prescribed margin dose were significant predictors. The post-SRS hemorrhage rate increased with larger bAVM volume only among the diffuse nidi (1.7 versus 14.9 versus 30.6 hemorrhage per 1000 person-years in bAVM volume < 20 cm³ versus 20–40 cm³ versus > 40 cm³; p = 0.022). The significantly higher post-SRS hemorrhage rate of Spetzler-Martin grade IV–V compared with grade I–III bAVMs (20.0 versus 3.3 hemorrhages per 1000 person-years; p = 0.001) mainly originated from the diffuse bAVMs rather than the compact subgroup (30.9 versus 4.8 hemorrhages per 1000 person-years; p = 0.035). Compact and smaller bAVMs, with higher prescribed margin dose harbor lower risks of post-SRS hemorrhage. The post-SRS hemorrhage rate exceeded 2.2% annually within the diffuse and large (> 40 cm³) bAVMs and the diffuse Spetzler-Martin IV–V bAVMs. These findings may help guide patient selection of SRS for the unruptured bAVMs.

Original language	English
Article number	4011
Pages (from-to)	4011
Journal	Scientific Reports
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41598-024-54369-2
Publication status	Published - Feb 18 2024

Keywords

Arteriovenous malformation morphology
Automated segmentation
Compactness index
Post-SRS hemorrhage
Stereotactic radiosurgery
Vascular disorders

ASJC Scopus subject areas

General

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10.1038/s41598-024-54369-2

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Huang, P. W., Peng, S. J., Pan, D. H. C., Yang, H. C., Tsai, J. T., Shiau, C. Y., Su, I. C., Chen, C. J., Wu, H. M., Lin, C. J., Chung, W. Y., Guo, W. Y., Lo, W. L., Lai, S. W., & Lee, C. C. (2024). Vascular compactness of unruptured brain arteriovenous malformation predicts risk of hemorrhage after stereotactic radiosurgery. Scientific Reports, 14(1), 4011. Article 4011. https://doi.org/10.1038/s41598-024-54369-2

Huang, PW , Peng, SJ, Pan, DHC, Yang, HC, Tsai, JT, Shiau, CY, Su, IC, Chen, CJ, Wu, HM, Lin, CJ, Chung, WY, Guo, WY, Lo, WL, Lai, SW & Lee, CC 2024, 'Vascular compactness of unruptured brain arteriovenous malformation predicts risk of hemorrhage after stereotactic radiosurgery', Scientific Reports, vol. 14, no. 1, 4011, pp. 4011. https://doi.org/10.1038/s41598-024-54369-2

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title = "Vascular compactness of unruptured brain arteriovenous malformation predicts risk of hemorrhage after stereotactic radiosurgery",

abstract = "The aim of the study was to investigate whether morphology (i.e. compact/diffuse) of brain arteriovenous malformations (bAVMs) correlates with the incidence of hemorrhagic events in patients receiving Stereotactic Radiosurgery (SRS) for unruptured bAVMs. This retrospective study included 262 adult patients with unruptured bAVMs who underwent upfront SRS. Hemorrhagic events were defined as evidence of blood on CT or MRI. The morphology of bAVMs was evaluated using automated segmentation which calculated the proportion of vessel, brain tissue, and cerebrospinal fluid in bAVMs on T2-weighted MRI. Compactness index, defined as the ratio of vessel to brain tissue, categorized bAVMs into compact and diffuse types based on the optimal cutoff. Cox proportional hazard model was used to identify the independent factors for post-SRS hemorrhage. The median clinical follow-ups was 62.1 months. Post-SRS hemorrhage occurred in 13 (5.0%) patients and one of them had two bleeds, resulting in an annual bleeding rate of 0.8%. Multivariable analysis revealed bAVM morphology (compact versus diffuse), bAVM volume, and prescribed margin dose were significant predictors. The post-SRS hemorrhage rate increased with larger bAVM volume only among the diffuse nidi (1.7 versus 14.9 versus 30.6 hemorrhage per 1000 person-years in bAVM volume < 20 cm3 versus 20–40 cm3 versus > 40 cm3; p = 0.022). The significantly higher post-SRS hemorrhage rate of Spetzler-Martin grade IV–V compared with grade I–III bAVMs (20.0 versus 3.3 hemorrhages per 1000 person-years; p = 0.001) mainly originated from the diffuse bAVMs rather than the compact subgroup (30.9 versus 4.8 hemorrhages per 1000 person-years; p = 0.035). Compact and smaller bAVMs, with higher prescribed margin dose harbor lower risks of post-SRS hemorrhage. The post-SRS hemorrhage rate exceeded 2.2% annually within the diffuse and large (> 40 cm3) bAVMs and the diffuse Spetzler-Martin IV–V bAVMs. These findings may help guide patient selection of SRS for the unruptured bAVMs.",

keywords = "Arteriovenous malformation morphology, Automated segmentation, Compactness index, Post-SRS hemorrhage, Stereotactic radiosurgery, Vascular disorders",

author = "Huang, {Po Wei} and Peng, {Syu Jyun} and Pan, {David Hung Chi} and Yang, {Huai Che} and Tsai, {Jo Ting} and Shiau, {Cheng Ying} and Su, {I. Chang} and Chen, {Ching Jen} and Wu, {Hsiu Mei} and Lin, {Chung Jung} and Chung, {Wen Yuh} and Guo, {Wan Yuo} and Lo, {Wei Lun} and Lai, {Shao Wen} and Lee, {Cheng Chia}",

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doi = "10.1038/s41598-024-54369-2",

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T1 - Vascular compactness of unruptured brain arteriovenous malformation predicts risk of hemorrhage after stereotactic radiosurgery

AU - Huang, Po Wei

AU - Peng, Syu Jyun

AU - Pan, David Hung Chi

AU - Yang, Huai Che

AU - Tsai, Jo Ting

AU - Shiau, Cheng Ying

AU - Su, I. Chang

AU - Chen, Ching Jen

AU - Wu, Hsiu Mei

AU - Lin, Chung Jung

AU - Chung, Wen Yuh

AU - Guo, Wan Yuo

AU - Lo, Wei Lun

AU - Lai, Shao Wen

AU - Lee, Cheng Chia

N1 - Publisher Copyright: © The Author(s) 2024.

PY - 2024/2/18

Y1 - 2024/2/18

N2 - The aim of the study was to investigate whether morphology (i.e. compact/diffuse) of brain arteriovenous malformations (bAVMs) correlates with the incidence of hemorrhagic events in patients receiving Stereotactic Radiosurgery (SRS) for unruptured bAVMs. This retrospective study included 262 adult patients with unruptured bAVMs who underwent upfront SRS. Hemorrhagic events were defined as evidence of blood on CT or MRI. The morphology of bAVMs was evaluated using automated segmentation which calculated the proportion of vessel, brain tissue, and cerebrospinal fluid in bAVMs on T2-weighted MRI. Compactness index, defined as the ratio of vessel to brain tissue, categorized bAVMs into compact and diffuse types based on the optimal cutoff. Cox proportional hazard model was used to identify the independent factors for post-SRS hemorrhage. The median clinical follow-ups was 62.1 months. Post-SRS hemorrhage occurred in 13 (5.0%) patients and one of them had two bleeds, resulting in an annual bleeding rate of 0.8%. Multivariable analysis revealed bAVM morphology (compact versus diffuse), bAVM volume, and prescribed margin dose were significant predictors. The post-SRS hemorrhage rate increased with larger bAVM volume only among the diffuse nidi (1.7 versus 14.9 versus 30.6 hemorrhage per 1000 person-years in bAVM volume < 20 cm3 versus 20–40 cm3 versus > 40 cm3; p = 0.022). The significantly higher post-SRS hemorrhage rate of Spetzler-Martin grade IV–V compared with grade I–III bAVMs (20.0 versus 3.3 hemorrhages per 1000 person-years; p = 0.001) mainly originated from the diffuse bAVMs rather than the compact subgroup (30.9 versus 4.8 hemorrhages per 1000 person-years; p = 0.035). Compact and smaller bAVMs, with higher prescribed margin dose harbor lower risks of post-SRS hemorrhage. The post-SRS hemorrhage rate exceeded 2.2% annually within the diffuse and large (> 40 cm3) bAVMs and the diffuse Spetzler-Martin IV–V bAVMs. These findings may help guide patient selection of SRS for the unruptured bAVMs.

AB - The aim of the study was to investigate whether morphology (i.e. compact/diffuse) of brain arteriovenous malformations (bAVMs) correlates with the incidence of hemorrhagic events in patients receiving Stereotactic Radiosurgery (SRS) for unruptured bAVMs. This retrospective study included 262 adult patients with unruptured bAVMs who underwent upfront SRS. Hemorrhagic events were defined as evidence of blood on CT or MRI. The morphology of bAVMs was evaluated using automated segmentation which calculated the proportion of vessel, brain tissue, and cerebrospinal fluid in bAVMs on T2-weighted MRI. Compactness index, defined as the ratio of vessel to brain tissue, categorized bAVMs into compact and diffuse types based on the optimal cutoff. Cox proportional hazard model was used to identify the independent factors for post-SRS hemorrhage. The median clinical follow-ups was 62.1 months. Post-SRS hemorrhage occurred in 13 (5.0%) patients and one of them had two bleeds, resulting in an annual bleeding rate of 0.8%. Multivariable analysis revealed bAVM morphology (compact versus diffuse), bAVM volume, and prescribed margin dose were significant predictors. The post-SRS hemorrhage rate increased with larger bAVM volume only among the diffuse nidi (1.7 versus 14.9 versus 30.6 hemorrhage per 1000 person-years in bAVM volume < 20 cm3 versus 20–40 cm3 versus > 40 cm3; p = 0.022). The significantly higher post-SRS hemorrhage rate of Spetzler-Martin grade IV–V compared with grade I–III bAVMs (20.0 versus 3.3 hemorrhages per 1000 person-years; p = 0.001) mainly originated from the diffuse bAVMs rather than the compact subgroup (30.9 versus 4.8 hemorrhages per 1000 person-years; p = 0.035). Compact and smaller bAVMs, with higher prescribed margin dose harbor lower risks of post-SRS hemorrhage. The post-SRS hemorrhage rate exceeded 2.2% annually within the diffuse and large (> 40 cm3) bAVMs and the diffuse Spetzler-Martin IV–V bAVMs. These findings may help guide patient selection of SRS for the unruptured bAVMs.

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KW - Automated segmentation

KW - Compactness index

KW - Post-SRS hemorrhage

KW - Stereotactic radiosurgery

KW - Vascular disorders

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Vascular compactness of unruptured brain arteriovenous malformation predicts risk of hemorrhage after stereotactic radiosurgery

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