Relationship between the features of venous drainage of supratentorial arteriovenous malformations and the risk of intracranial hemorrhage

Mamonov N.A.; Samochernyh K.A.

doi:https://doi.org/10.17116/neiro202286041104

Close metadata

BACKGROUND

Intracranial hemorrhage is the most common complication of cerebral arteriovenous malformations (AVM). In recent years, most studies devoted to the features of AVM functioning consider venous drainage as important factor influencing the rupture of malformation.

OBJECTIVE

To review the literature data on the relationship between the features of venous drainage of cerebral arteriovenous malformations and intracranial hemorrhage.

MATERIAL AND METHODS

We found 43 studies discussing the features of AVM venous drainage for the period from 1982 to 2020. Most of reports were published between 2005 and 2020.

RESULTS

Deep venous drainage and a single drainage vein were the most significant factors influencing the risk of hemorrhage. Venous ectasia, reflux, stenosis, number, length and tortuosity of drainage veins were less important for the risk of AVM rupture.

CONCLUSION

Analysis of the features of AVM venous drainage can make it possible to predict the natural course of disease and risk of intracranial hemorrhage. These aspects are essential for neurosurgical treatment.

Keywords:

arteriovenous malformation

venous drainage

intracranial hemorrhage

Authors:

Mamonov N.A.

Polenov Research Neurosurgery Institute

Samochernyh K.A.

Polenov Russian Research Institute of Neurosurgery – a branch of the Almazov National Medical Research Centre of the Ministry of Health of the Russian Federation

ORCID: 0000-0003-0350-0249

Received:

01.12.2021

Accepted:

10.06.2022

Close metadata

References:

Abecassis IJ, Xu DS, Batjer HH, Bendok BR. Natural history of brain arteriovenous malformations: a systematic review. Neurosurgical Focus. 2014;37(3): E7. https://doi.org/10.3171/2014.6.FOCUS14250
Baharvahdat H, Blanc R, Termechi R, Pistocchi S, Bartolini B, Redjem H, Piotin M. Hemorrhagic complications after endovascular treatment of cerebral arteriovenous malformations. AJNR. American Journal of Neuroradiology. 2014;35(5):978-983. https://doi.org/10.3174/ajnr.A3906
Mohr JP, Overbey JR, Hartmann A, Kummer RV, Al-Shahi Salman R, Kim H, van der Worp HB, Parides MK, Stefani MA, Houdart E, Libman R, Pile-Spellman J, Harkness K, Cordonnier C, Moquete E, Biondi A, Klijn CJM, Stapf C, Moskowitz AJ; ARUBA co-investigators. Medical management with interventional therapy versus medical management alone for unruptured brain arteriovenous malformations (ARUBA): final follow-up of a multicentre, non-blinded, randomized controlled trial. The Lancet. Neurology. 2020;19(7):573-581. https://doi.org/10.1016/S1474-4422(20)30181-2
Mohr JP, Kejda-Scharler J, Pile-Spellman J. Diagnosis and treatment of arteriovenous malformations. Current Neurology and Neuroscience Reports. 2013;13(2):324. https://doi.org/10.1007/s11910-012-0324-1
Rutledge WC, Ko NU, Lawton MT, Kim H. Hemorrhage rates and risk factors in the natural history course of brain arteriovenous malformations. Translational Stroke Research. 2014;5(5):538-542. https://doi.org/10.1007/s12975-014-0351-0
Miyasaka Y, Yada K, Ohwada T, Kitahara T, Kurata A, Irikura K. An analysis of the venous drainage system as a factor in hemorrhage from arteriovenous malformations. Journal of Neurosurgery. 1992;76(2):239-243. https://doi.org/10.3171/jns.1992.76.2.0239
Alexander MD, Cooke DL, Nelson J, Guo DE, Dowd CF, Higashida RT, Halbach VV, Lawton MT, Kim H, Hetts SW. Association between Venous Angioarchitectural Features of Sporadic Brain Arteriovenous Malformations and Intracranial Hemorrhage. AJNR. American Journal of Neuroradiology. 2015;36(5):949-952. https://doi.org/10.3174/ajnr.A4224
Derdeyn CP, Zipfel GJ, Albuquerque FC, Cooke DL, Feldmann E, Sheehan JP, Torner JC; American Heart Association Stroke Council. Management of Brain Arteriovenous Malformations: A Scientific Statement for Healthcare Professionals from the American Heart Association/American Stroke Association. Stroke. 2017;48(8):e200-e224. https://doi.org/10.1161/STR.0000000000000134
Samochernyh KA. Arteriovenoznye mal’formacii polusharij bol’shogo mozga u detej. (Voprosy diagnostiki i rezul’taty hirurgicheskogo lecheniya). Avtoreferat dis. … kand. med. nauk. Sankt-Peterburg, 2002. (In Russ.).
Goldberg J, Raabe A, Bervini D. Natural history of brain arteriovenous malformations: systematic review. Journal of Neurosurgical Sciences. 2018;62(4):437-443. https://doi.org/10.23736/S0390-5616.18.04452-1
Lawton MT, Rutledge WC, Kim H, Stapf C, Whitehead KJ, Li DY, Krings T, terBrugge K, Kondziolka D, Morgan MK, Moon K, Spetzler RF.Brain arteriovenous malformations. Nature Reviews. Disease Primers. 2015;1:15008. https://doi.org/10.1038/nrdp.2015.8
Hachatryan VA, Samochernyh KA, Trofimova TN. Cerebrovaskulyarnaya patologiya u detej. SPb.: Desyatka; 2006. (In Russ.).
Ding D, Starke RM, Kano H, Mathieu D, Huang PP, Feliciano C, Rodriguez-Mercado R, Almodovar L, Grills IS, Silva D, Abbassy M, Missios S, Kondziolka D, Barnett GH, Dade Lunsford L, Sheehan JP. International multicenter cohort study of pediatric brain arteriovenous malformations. Part 1: Predictors of hemorrhagic presentation. Journal of Neurosurgery. Pediatrics. 2017;19(2):127-135. https://doi.org/10.3171/2016.9.PEDS16283
Osbun JW, Reynolds MR, Barrow DL. Arteriovenous malformations: epidemiology, clinical presentation, and diagnostic evaluation. Handbook of Clinical Neurology. 2017;143:25-29. https://doi.org/10.1016/B978-0-444-63640-9.00003-5
Gross BA, Du R. Natural history of cerebral arteriovenous malformations: a meta-analysis. Journal of Neurosurgery. 2013;118(2):437-443. https://doi.org/10.3171/2012.10.JNS121280
Hernesniemi JA, Dashti R, Juvela S, Väärt K, Niemelä M, Laakso A. Natural history of brain arteriovenous malformations: a long-term follow-up study of risk of hemorrhage in 238 patients. Neurosurgery. 2008;63(5):823-831. https://doi.org/10.1227/01.NEU.0000330401.82582.5E
Kim H, Al-Shahi Salman R, McCulloch CE, Stapf C, Young WL; MARS Coinvestigators. Untreated brain arteriovenous malformation: patient-level meta-analysis of hemorrhage predictors. Neurology. 2014;83(7):590-597. https://doi.org/10.1212/WNL.0000000000000688
Rangel-Castilla L, Russin JJ, Martinez-Del-Campo E, Soriano-Baron H, Spetzler RF, Nakaji P. Molecular and cellular biology of cerebral arteriovenous malformations: a review of current concepts and future trends in treatment. Neurosurgical Focus. 2014;37(3):E1. https://doi.org/10.3171/2014.7.FOCUS14214
Choi JH, Mohr JP. Brain arteriovenous malformations in adults. The Lancet. Neurology. 2005;4(5):299-308. https://doi.org/10.1016/S1474-4422(05)70073-9
Rozhchenko LV. Molecular mechanisms of growth and relapse of cerebral arteriovenous malformations. Voprosy nejrohirurgii imeni N.N. Burdenko. 2020;84(1):94-100. (In Russ.). https://doi.org/10.17116/neiro20208401194
Samochernyh KA. Arteriovenous malformations of the subtentorial localization of the brain in children. Nejrohirurgiya i nevrologiya detskogo vozrasta. 2001;3:49. (In Russ.).
Krings T, Hans FJ, Geibprasert S, Terbrugge K. Partial “targeted” embolisation of brain arteriovenous malformations. European Radiology. 2010;20(11):2723-2731. https://doi.org/10.1007/s00330-010-1834-3
Mikhak B, Weinsheimer S, Pawlikowska L, Poon A, Kwok PY, Lawton MT, Chen Y, Zaroff JG, Sidney S, McCulloch CE, Young WL, Kim H. Angiopoietin-like 4 (ANGPTL4) gene polymorphisms and risk of brain arteriovenous malformations. Cerebrovascular Diseases (Basel, Switzerland). 2011;31(4):338-345. https://doi.org/10.1159/000322601
da Costa L, Wallace MC, Ter Brugge KG, O’Kelly C, Willinsky RA, Tymianski M. The natural history and predictive features of hemorrhage from brain arteriovenous malformations. Stroke. 2009;40(1):100-105. https://doi.org/10.1161/STROKEAHA.108.524678
Yamada S, Takagi Y, Nozaki K, Kikuta K, Hashimoto N. Risk factors for subsequent hemorrhage in patients with cerebral arteriovenous malformations. Journal of Neurosurgery. 2007;107(5):965-972. https://doi.org/10.3171/JNS-07/11/0965
Stapf C, Mast H, Sciacca RR, Choi JH, Khaw AV, Connolly ES, Pile-Spellman J, Mohr JP. Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology. 2006;66(9):1350-1355. https://doi.org/10.1212/01.wnl.0000210524.68507.87
Pan J, Feng L, Vinuela F, He H, Wu Z, Zhan R. Angioarchitectural characteristics associated with initial hemorrhagic presentation in supratentorial brain arteriovenous malformations. European Journal of Radiology. 2013;82(11):1959-1963. https://doi.org/10.1016/j.ejrad.2013.05.015
Albert P. Personal experience in the treatment of 178 cases of arteriovenous malformations of the brain. Acta Neurochirurgica. 1982;61(1-3):207-226. https://doi.org/10.1007/BF01740086
Ji Y, Ding X, Wang ZG. [Analysis of relevant factors of cerebral arteriovenous malformation with hemorrhage]. Zhonghua Yi Xue Za Zhi. 2012;92(35):2488-2490.
Kubalek R, Moghtaderi A, Klisch J, Berlis A, Quiske A, Schumacher M. Cerebral arteriovenous malformations: influence of angioarchitecture on bleeding risk. Acta Neurochirurgica. 2003;145(12):1045-1052. https://doi.org/10.1007/s00701-003-0143-x
Lv X, Wu Z, Jiang C, Yang X, Li Y, Sun Y, Zhang N. Angioarchitectural characteristics of brain arteriovenous malformations with and without hemorrhage. World Neurosurgery. 2011;76(1-2):95-99. https://doi.org/10.1016/j.wneu.2011.01.044
Niu H, Cao Y, Wang X, Xue X, Yu L, Yang M, Wang R. Relationships between hemorrhage, angioarchitectural factors and collagen of arteriovenous malformations. Neuroscience Bulletin. 2012;28(5):595-605. https://doi.org/10.1007/s12264-012-1271-1
Bai J, Dou CW, Wang YJ, Liu L, Zhao JZ, Wang S, Zhao YL. [Correlations of angio-architectural factors with cerebral arteriovenous malformation hemorrhage]. Zhonghua Yi Xue Za Zhi. 2012;92(31):2202-2204.
Brunozzi D, Theiss P, Amin-Hanjani S, Charbel FT, Mohammaden M, Andrews A, Linninger A, Alaraj A. Ratio of Arteriovenous Malformation Draining Vein to Adjacent Venous Sinus Diameter Is Associated with Increased Risk of Venous Stenosis. World Neurosurgery. 2019;130:e1111-1115. https://doi.org/10.1016/j.wneu.2019.07.100
Mansmann U, Meisel J, Brock M, Rodesch G, Alvarez H, Lasjaunias P. Factors associated with intracranial hemorrhage in cases of cerebral arteriovenous malformation. Neurosurgery. 2000;46(2): 272-281. https://doi.org/10.1097/00006123-200002000-00004
Yu JF, Nicholson AD, Nelson J, Alexander MD, Tse SH, Hetts SW, Hemphill JC 3rd, Kim H, Cooke DL. Predictors of intracranial hemorrhage volume and distribution in brain arteriovenous malformation. Interventional Neuroradiology. 2018;24(2):183-188. https://doi.org/10.1177/1591019917749819
Alqadi M, Brunozzi D, Linninger A, Amin-Hanjani S, Charbel FT, Alaraj A. Cerebral arteriovenous malformation venous stenosis is associated with hemodynamic changes at the draining vein-venous sinus junction. Medical Hypotheses. 2019;123:86-88. https://doi.org/10.1016/j.mehy.2019.01.003
de Castro-Afonso LH, Vanzim JR, Trivelato FP, Rezende MT, Ulhôa AC, Chodraui-Filho SF, de Abreu Mattos LG, Mounayer C, Nakiri GS, Colli BO, Abud DG; IntraCranial Arteriovenous RUpture riSk Study (ICARUSS) investigators. Association between draining vein diameters and intracranial arteriovenous malformation hemorrhage: a multicentric retrospective study. Neuroradiology. 2020;62(11):1497-1505. https://doi.org/10.1007/s00234-020-02484-y
Telischak NA, Yedavalli V, Massoud TF. Tortuosity of superior cerebral veins: Comparative magnetic resonance imaging morphometrics in normal subjects and arteriovenous malformation patients. Clinical Anatomy. 2021;34(3):326-332. https://doi.org/10.1002/ca.23589
Batjer HH, Devous MD, Seibert GB, Purdy PD, Bonte FJ. Intracranial arteriovenous malformations: relationship between clinical factors and surgical complications. Neurosurgery. 1989;24(1):75-79. https://doi.org/10.1227/00006123-198901000-00012
al-Rodhan NR, Sundt TM Jr, Piepgras DG, Nichols DA, Rüfenacht D, Stevens LN. Occlusive hyperemia: a theory for the hemodynamic complications following resection of intracerebral arteriovenous malformations. Journal of Neurosurgery. 1993;78(2):167-175. https://doi.org/10.3171/jns.1993.78.2.0167
D’Aliberti G, Talamonti G, Piparo M, Debernardi A, Zella S, Boccardi E, Valvassori L, Nichelatti M. Venous flow rearrangement after treatment of cerebral arteriovenous malformations: a novel approach to evaluate the risks of treatment. World Neurosurgery. 2014;82(1-2):160-169. https://doi.org/10.1016/j.wneu.2013.02.005
Shekhtman OD, Maryashev SA, Eliava SS, Yakovlev SB, Golanov AV, Shishkina LV, Pilipenko YuV, Okishev DN, Bocharov AV, Buharin EYu, Mikeladze KG, Kisar’ev SA, Vinogradov EV, Kaftanov AN, Konovalov AN. Combined treatment of cerebral arteriovenous malformations. Experience of the Burdenko Neurosurgical Institute. Voprosy nejrohirurgii imeni N.N. Burdenko. 2015;79(4):4-18. (In Russ.). https://doi.org/10.17116/neiro20157944-18