Stereotactic radiosurgery (SRS) for patients with brainstem cerebral cavernous malformations (CCMs): an international, multicentric study.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
29 10 2024
Historique:
received: 11 02 2024
accepted: 21 10 2024
medline: 30 10 2024
pubmed: 30 10 2024
entrez: 30 10 2024
Statut: epublish

Résumé

Brainstem cerebral cavernous malformations (CCM) are clinically more aggressive compared to superficial CCMs. Due to their location, resection can be challenging, making stereotactic radiosurgery (SRS) an attractive alternative for symptomatic patient. Brainstem CCM patients (n = 170) were treated with Gamma Knife SRS at 11 radiosurgical centers. Hemorrhagic risk reduction, risk factors of post-SRS hemorrhage, and clinical outcomes were retrospectively analyzed. Most patients had a single (165/170 patients) brainstem CCMs treated; the majority of CCMs (165/181) presented with bleeding. Single-session SRS decreased the risk of repeat hemorrhage in patients with hemorrhagic brainstem CCM (HR: 0.17, p < 0.001) using recurrent multivariate analysis. The annual hemorrhage rate decreased from 14.8 per 100 CCM-years before SRS to 2.3 after treatment. Using univariate Cox-analysis, the probability of a new hemorrhages after SRS was reduced for patient older than 35 years (HR = 0.21, p = 0.002) and increased with a margin dose > 13 Gy (HR = 2.57, p = 0.044). Adverse radiation effect (ARE) occurred in 9 patients (5.3%) and was symptomatic in four (2.4%). At a median follow-up of 3.4 years (Inter-quartile range: 5.4), 13 patients (8.0%) had a worsened clinical status, with the treated CCM being the cause in 5.6% (10) of the patients. Single-session SRS decreased the risk of repeat hemorrhage in patients with hemorrhagic brainstem CCM and conveyed this benefit with a low risk of advrse radiation effects (ARE) and worsening clinical status.

Identifiants

pubmed: 39472707
doi: 10.1038/s41598-024-77140-z
pii: 10.1038/s41598-024-77140-z
doi:

Types de publication

Journal Article Multicenter Study

Langues

eng

Sous-ensembles de citation

IM

Pagination

25933

Informations de copyright

© 2024. The Author(s).

Références

Gross, B. A., Batjer, H. H., Awad, I. A., Bendok, B. R. & Du, R. Brainstem cavernous malformations: 1390 surgical cases from the literature. World Neurosurg. 80(1–2), 89–93. https://doi.org/10.1016/j.wneu.2012.04.002 (2013).
doi: 10.1016/j.wneu.2012.04.002 pubmed: 22484766
Porter, R. W. et al. Cavernous malformations of the brainstem: Experience with 100 patients. J. Neurosurg. 90(1), 50–58. https://doi.org/10.3171/jns.1999.90.1.0050 (1999).
doi: 10.3171/jns.1999.90.1.0050 pubmed: 10413155
Horne, M. A. et al. Clinical course of untreated cerebral cavernous malformations: A meta-analysis of individual patient data. Lancet Neurol.Bold">15(2), 166–173. https://doi.org/10.1016/S1474-4422(15)00303-8 (2016).
doi: 10.1016/S1474-4422(15)00303-8 pubmed: 26654287 pmcid: 4710581
Garcia R.M., Ivan M.E., & Lawton, M.T. Brainstem cavernous malformations: Surgical results in 104 patients and a proposed grading system to predict neurological outcomes. Neurosurgery. 76(3), 265–277. https://doi.org/10.1227/NEU.0000000000000602 (2015). discussion 277–278.
Fritschi, J. A., Reulen, H. J., Spetzler, R. F. & Zabramski, J. M. Cavernous malformations of the brain stem. A review of 139 cases. Acta Neurochir. (Wien). 130(1–4), 35–46. https://doi.org/10.1007/BF01405501 (1994).
doi: 10.1007/BF01405501 pubmed: 7725941
Pandey, P., Westbroek, E., Gooderham, P. & Steinberg, G. Cavernous malformation of Brainstem, Thalamus, and basal ganglia: A series of 176 patients. NEUROSURGERY. 72(4), 573–588. https://doi.org/10.1227/NEU.0b013e318283c9c2 (2013).
doi: 10.1227/NEU.0b013e318283c9c2 pubmed: 23262564
Kondziolka, D., Lunsford, L. D., Coffey, R. J., Bissonette, D. J. & Flickinger, J. C. Stereotactic radiosurgery of angiographically occult vascular malformations: indications and preliminary experience. Neurosurgery. 27(6), 892–900. https://doi.org/10.1097/00006123-199012000-00006 (1990).
doi: 10.1097/00006123-199012000-00006 pubmed: 2274130
Akers, A., Al-Shahi Salman, R. & Awad, A. Synopsis of guidelines for the Clinical Management of Cerebral cavernous malformations: Consensus recommendations based on Systematic Literature Review by the Angioma Alliance Scientific Advisory Board Clinical Experts Panel. Neurosurgery. 80(5), 665. https://doi.org/10.1093/neuros/nyx091 (2017).
doi: 10.1093/neuros/nyx091 pubmed: 28387823 pmcid: 5808153
von Elm, E. et al. The strengthening the reporting of Observational studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies. J. Clin. Epidemiol. 61(4), 344–349. https://doi.org/10.1016/j.jclinepi.2007.11.008 (2008).
doi: 10.1016/j.jclinepi.2007.11.008
Al-Shahi Salman, R., Berg, M. J., Morrison, L., Awad, I. A. & Angioma Alliance Scientific Advisory Board. Hemorrhage from cavernous malformations of the brain: definition and reporting standards. Angioma Alliance Sci. Advisory Board. Stroke. 39(12), 3222–3230. https://doi.org/10.1161/STROKEAHA.108.515544 (2008).
doi: 10.1161/STROKEAHA.108.515544
Zabramski, J. M. et al. The natural history of familial cavernous malformations: Results of an ongoing study. J. Neurosurg. 80(3), 422–432. https://doi.org/10.3171/jns.1994.80.3.0422 (1994).
doi: 10.3171/jns.1994.80.3.0422 pubmed: 8113854
Dumot, C. et al. Stereotactic radiosurgery for haemorrhagic cerebral cavernous malformation: A multi-institutional, retrospective study. Stroke Vasc Neurol. Published online. doi: (2023). https://doi.org/10.1136/svn-2023-002380
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL (2020). https://www.R-project.org/
RStudio, T. & RStudio RStudio: Integrated Development Environment for R. PBC, Boston, MA URL http://www.rstudio.com/ . (2020).
Sahai, H. & Khurshid, A. Statistics in Epidemiology: Methods, Techniques, and Applications (CRC, 1996).
Amorim, L. D. A. F. & Cai, J. Modelling recurrent events: a tutorial for analysis in epidemiology. Int. J. Epidemiol. 44(1), 324–333. https://doi.org/10.1093/ije/dyu222 (2015).
doi: 10.1093/ije/dyu222 pubmed: 25501468
Moeller, B. J., Cao, Y., Li, C. Y. & Dewhirst, M. W. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell. 5(5), 429–441. https://doi.org/10.1016/s1535-6108(04)00115-1 (2004).
doi: 10.1016/s1535-6108(04)00115-1 pubmed: 15144951
Park, C. M. et al. Ionizing radiation enhances matrix metalloproteinase-2 secretion and invasion of glioma cells through Src/epidermal growth factor receptor-mediated p38/Akt and phosphatidylinositol 3-kinase/Akt signaling pathways. Cancer Res. 66(17), 8511–8519. https://doi.org/10.1158/0008-5472.CAN-05-4340 (2006).
doi: 10.1158/0008-5472.CAN-05-4340 pubmed: 16951163
Hlatky, L., Tsionou, C., Hahnfeldt, P. & Coleman, C. N. Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res. 54(23), 6083–6086 (1994).
pubmed: 7525053
Gross, B. A. & Du, R. Hemorrhage from cerebral cavernous malformations: a systematic pooled analysis. J. Neurosurg. 126(4), 1079–1087. https://doi.org/10.3171/2016.3.JNS152419 (2017).
doi: 10.3171/2016.3.JNS152419 pubmed: 27203143
Grunewald, M. et al. Counteracting age-related VEGF signaling insufficiency promotes healthy aging and extends life span. Science. 373(6554), eabc8479. https://doi.org/10.1126/science.abc8479 (2021).
doi: 10.1126/science.abc8479 pubmed: 34326210
Pollock, B. E. et al. Stereotactic radiosurgery for cavernous malformations. J. Neurosurg. 93(6), 987–991. https://doi.org/10.3171/jns.2000.93.6.0987 (2000).
doi: 10.3171/jns.2000.93.6.0987 pubmed: 11117872
Lunsford, L. D., Niranjan, A., Kano, H., Monaco Iii, E. A. & Flickinger, J. C. Leksell Stereotactic Radiosurgery for cavernous malformations. Prog Neurol. Surg. 34, 260–266. https://doi.org/10.1159/000493072 (2019).
doi: 10.1159/000493072 pubmed: 31096254
Nagy, G. et al. Contemporary radiosurgery of cerebral cavernous malformations: Part 1. Treatment outcome for critically located hemorrhagic lesions. J. Neurosurg. 1306(6), 1817–1825. https://doi.org/10.3171/2017.5.JNS17776 (2019).
doi: 10.3171/2017.5.JNS17776
Karaaslan, B. et al. Stereotactic radiosurgery for cerebral cavernous malformation: Comparison of hemorrhage rates before and after stereotactic radiosurgery. J. Neurosurg. 136(3), 655–661. https://doi.org/10.3171/2021.2.JNS21138 (2022).
doi: 10.3171/2021.2.JNS21138 pubmed: 34450585
Xu, X. Y. et al. Nomogram for predicting an individual prospective hemorrhage risk in untreated brainstem cavernous malformations. J. Neurosurg. 138(4), 910–921. https://doi.org/10.3171/2022.8.JNS221228 (2023).
doi: 10.3171/2022.8.JNS221228 pubmed: 36152323
Hori, T. et al. Long-term outcomes after surgery for brainstem cavernous malformations: Analysis of 46 consecutive cases. J. Neurosurg. 138(4), 900–909. https://doi.org/10.3171/2022.7.JNS22314 (2023).
doi: 10.3171/2022.7.JNS22314 pubmed: 36087317
Walcott, B. P., Choudhri, O. & Lawton, M. T. Brainstem cavernous malformations: Natural history versus surgical management. J. Clin. Neurosci. 32, 164–165. https://doi.org/10.1016/j.jocn.2016.03.021 (2016).
doi: 10.1016/j.jocn.2016.03.021 pubmed: 27320373 pmcid: 5011020
Niranjan, A. & Lunsford, L. D. Stereotactic radiosurgery guidelines for the management of patients with intracranial cavernous malformations. Prog Neurol. Surg. 27, 166–175. https://doi.org/10.1159/000341792 (2013).
doi: 10.1159/000341792 pubmed: 23258521
Li, D. et al. Neurological outcomes of untreated brainstem cavernous malformations in a prospective observational cohort and literature review. Stroke Vasc Neurol. 6(4), 501–510. https://doi.org/10.1136/svn-2020-000608 (2021).
doi: 10.1136/svn-2020-000608 pubmed: 33737399 pmcid: 8717781
Li, D. et al. Natural history of brainstem cavernous malformations: Prospective hemorrhage rate and adverse factors in a consecutive prospective cohort. J. Neurosurg. 134(3), 917–928. https://doi.org/10.3171/2019.12.JNS192856 (2021).
doi: 10.3171/2019.12.JNS192856 pubmed: 32168479

Auteurs

Sam Dayawansa (S)

Department of Neurological Surgery, University of Virginia, Box 800212, Charlottesville, VA, 22908, USA. samwansa20@gmail.com.

Chloe Dumot (C)

Department of Neurological Surgery, University of Virginia, Box 800212, Charlottesville, VA, 22908, USA.
Department of Neurological Surgery, Hospices Civils de Lyon, Lyon, France.

Georgios Mantziaris (G)

Department of Neurological Surgery, University of Virginia, Box 800212, Charlottesville, VA, 22908, USA.

Zhiyuan Xu (Z)

Department of Neurological Surgery, University of Virginia, Box 800212, Charlottesville, VA, 22908, USA.

Stylianos Pikis (S)

Department of Neurological Surgery, University of Virginia, Box 800212, Charlottesville, VA, 22908, USA.

Selcuk Peker (S)

Department of Neurosurgery, Koc University School of Medicine, Istanbul, Turkey.

Yavuz Samanci (Y)

Department of Neurosurgery, Koc University School of Medicine, Istanbul, Turkey.

Gokce D Ardor (GD)

Department of Neurosurgery, Koc University School of Medicine, Istanbul, Turkey.

Ahmed M Nabeel (AM)

Gamma Knife Center Cairo, Nasser Institute Hospital, Cairo, Egypt.
Neurosurgery Department, Faculty of Medicine, Benha University, Qalubya, Egypt.

Wael A Reda (WA)

Gamma Knife Center Cairo, Nasser Institute Hospital, Cairo, Egypt.
Department of Neurosurgery, Ain Shams University, Cairo, Egypt.

Sameh R Tawadros (SR)

Gamma Knife Center Cairo, Nasser Institute Hospital, Cairo, Egypt.
Department of Neurosurgery, Ain Shams University, Cairo, Egypt.

Khaled Abdelkarim (K)

Gamma Knife Center Cairo, Nasser Institute Hospital, Cairo, Egypt.
Department of Clinical Oncology, Ain Shams University, Cairo, Egypt.

Amr M N El-Shehaby (AMN)

Gamma Knife Center Cairo, Nasser Institute Hospital, Cairo, Egypt.
Department of Neurosurgery, Ain Shams University, Cairo, Egypt.

Reem M Emad Eldin (RME)

Gamma Knife Center Cairo, Nasser Institute Hospital, Cairo, Egypt.
Department of Radiation Oncology, National Cancer Institute, Cairo University, Cairo, Egypt.

Ahmed H Elazzazi (AH)

Extended Modular Program- Faculty of Medicine, Ain Shams University, Cairo, Egypt.

Nuria Martínez Moreno (NM)

Department of Radiosurgery, Rúber Internacional Hospital, Madrid, Spain.

Roberto Martínez Álvarez (RM)

Department of Radiosurgery, Rúber Internacional Hospital, Madrid, Spain.

Roman Liscak (R)

Department of Stereotactic and Radiation Neurosurgery, Na Homolce Hospital, Prague, Czech Republic.

Jaromir May (J)

Department of Stereotactic and Radiation Neurosurgery, Na Homolce Hospital, Prague, Czech Republic.

David Mathieu (D)

Division of Neurosurgery, Université de Sherbrooke, Centre de Recherche du CHUS, Sherbrooke, QC, Canada.

Jean-Nicolas Tourigny (JN)

Division of Neurosurgery, Université de Sherbrooke, Centre de Recherche du CHUS, Sherbrooke, QC, Canada.

Manjul Tripathi (M)

Department of Neurosurgery, Postgraduate Institute of Medical Education and Research, Chandigarh, India.

Akshay Rajput (A)

Department of Neurosurgery, Postgraduate Institute of Medical Education and Research, Chandigarh, India.

Narendra Kumar (N)

Department of Radiation Therapy, Postgraduate Institute of Medical Education and Research, Chandigarh, India.

Rupinder Kaur (R)

Department of Neurosurgery, Postgraduate Institute of Medical Education and Research, Chandigarh, India.

Piero Picozzi (P)

Department of Neurosurgery, Scientific Institute for Research, Hospitalization and Healthcare - IRCCS Humanitas Research Hospital, Milan, Italy.

Andrea Franzini (A)

Department of Neurosurgery, Scientific Institute for Research, Hospitalization and Healthcare - IRCCS Humanitas Research Hospital, Milan, Italy.

Herwin Speckter (H)

Dominican Gamma Knife Center and Radiology Department, CEDIMAT, Santo Domingo, Dominican Republic.

Wenceslao Hernandez (W)

Dominican Gamma Knife Center and Radiology Department, CEDIMAT, Santo Domingo, Dominican Republic.

Anderson Brito (A)

Dominican Gamma Knife Center and Radiology Department, CEDIMAT, Santo Domingo, Dominican Republic.

Ronald E Warnick (RE)

Gamma Knife Center, Jewish Hospital, Mayfield Clinic, Cincinnati, OH, USA.

Juan Alzate (J)

Department of Neurosurgery, NYU Langone, New York City, NY, USA.

Douglas Kondziolka (D)

Department of Neurosurgery, NYU Langone, New York City, NY, USA.

Greg N Bowden (GN)

Department of Neurosurgery and Department of Oncology, University of Alberta, Edmonton, AB, Canada.

Samir Patel (S)

Division of Radiation Oncology, Department of Oncology, University of Alberta, Edmonton, AB, Canada.

Jason P Sheehan (JP)

Department of Neurological Surgery, University of Virginia, Box 800212, Charlottesville, VA, 22908, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH