A Systematic Review of Cerebral Arteriovenous Malformation Management
DOI:
https://doi.org/10.5195/ijms.2017.13Keywords:
Intracranial Arteriovenous Malformations, Hemangioma, Cavernous, Central Nervous System, Precision Medicine, Gene Knockout Techniques, Patient SelectionAbstract
Cerebral Arteriovenous Malformation is a neurovascular lesion characterized by an abnormal connection between arterial and venous systems, resulting in a tangle of blood vessels lacking intervening capillaries. The goal of treatment is to prevent catastrophic hemorrhage, neurological injury, or death. Despite the availability of multiple cutting-edge treatment options there is little consensus on the most promising approaches for treatment due to the novelty of each Arteriovenous Malformation case. This analysis will link the various angioarchitectural characteristics and associated presentations of Arteriovenous Malformation to treatment modalities. In the era of personalized medicine, genomics-driven research to normalize by drawing parallels between Cerebral Cavernous Malformation and Arteriovenous Malformation, both of which are characterized by hemorrhage-prone vascular malformations, may provide insight for the development of pharmacological therapy. Understanding the underlying mechanisms and genes responsible for the symptoms will allow us to better treat patients in a non-invasive manner and paves future directions in Arteriovenous Malformation treatment.
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1. Al-Shahi R, Warlow C. A systematic review of the frequency and prognosis of arteriovenous malformations of the brain in adults. Brain. 2001; 124(Pt 10): 1900-26.
2. Brown RD, Jr., Wiebers DO, Forbes G, O'Fallon WM, Piepgras DG, Marsh WR, et al. The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg. 1988; 68(3): 352-7.
3. Zhao J, Wang S, Li J, Qi W, Sui D, Zhao Y. Clinical characteristics and surgical results of patients with cerebral arteriovenous malformations. Surgical neurology. 2005; 63(2): 156-61; discussion 61. eng
4. Martinez JL, Macdonald RL. Surgical Strategies for Acutely Ruptured Arteriovenous Malformations. Frontiers of neurology and neuroscience. 2015; 37: 166-81. eng
5. Murakami K, Endo T, Tominaga T. An analysis of flow dynamics in cerebral cavernous malformation and orbital cavernous angioma using indocyanine green videoangiography. Acta Neurochir (Wien). 2012; 154(7): 1169-75.
6. Gupta A, Periakaruppan A. Intracranial dural arteriovenous fistulas: A Review. Indian J Radiol Imaging. 2009; 19(1): 43-8.
7. Pabaney AH, Robin AM, Basheer A, Malik G. Surgical Management of Dural Arteriovenous Fistula After Craniotomy: Case Report and Review of Literature. World neurosurgery. 2016; 89: 731 e7- e11.
8. Lee JY, Son YJ, Kim JE. Intracranial pial arteriovenous fistulas. J Korean Neurosurg Soc. 2008; 44(2): 101-4.
9. Rohit, Goh PS. Diffuse Proliferative Cerebral Angiopathy: A case report and review of the literature. J Radiol Case Rep. 2015; 9(9): 1-10.
10. Guey S, Tournier-Lasserve E, Herve D, Kossorotoff M. Moyamoya disease and syndromes: from genetics to clinical management. Appl Clin Genet. 2015; 8: 49-68.
11. Pearl M, Gomez J, Gregg L, Gailloud P. Endovascular management of vein of Galen aneurysmal malformations. Influence of the normal venous drainage on the choice of a treatment strategy. Childs Nerv Syst. 2010; 26(10): 1367-79.
12. Berman MF, Sciacca RR, Pile-Spellman J, Stapf C, Connolly ES, Jr., Mohr JP, et al. The epidemiology of brain arteriovenous malformations. Neurosurgery. 2000; 47(2): 389-96; discussion 97.
13. Kim H, Su H, Weinsheimer S, Pawlikowska L, Young WL. Brain arteriovenous malformation pathogenesis: a response-to-injury paradigm. Acta Neurochir Suppl. 2011; 111: 83-92.
14. Carl J. Graf, George E. Perret, James C. Torner. Bleeding from cerebral arteriovenous malformations as part of their natural history. Journal of Neurosurgery. 1983; 58(3): 331-7.
15. Crawford PM, West CR, Chadwick DW, Shaw MD. Arteriovenous malformations of the brain: natural history in unoperated patients. J Neurol Neurosurg Psychiatry. 1986; 49(1): 1-10.
16. Forster DM, Steiner L, Hakanson S. Arteriovenous malformations of the brain. A long-term clinical study. J Neurosurg. 1972; 37(5): 562-70.
17. Mast H, Young WL, Koennecke HC, Sciacca RR, Osipov A, Pile-Spellman J, et al. Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation. Lancet. 1997; 350(9084): 1065-8.
18. Radvany MG, Gregg L. Endovascular treatment of cranial arteriovenous malformations and dural arteriovenous fistulas. Neurosurgery clinics of North America. 2012; 23(1): 123-31.
19. Stephen L. Ondra, Henry Troupp, Eugene D. George, Karen Schwab. The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. Journal of Neurosurgery. 1990; 73(3): 387-91.
20. Youichi Itoyama, Syouzaburou Uemura, Yukitaka Ushio, Jun-Ichi Kuratsu, Nobuhito Nonaka, Hidetaka Wada, et al. Natural course of unoperated intracranial arteriovenous malformations: study of 50 cases. Journal of Neurosurgery. 1989; 71(6): 805-9.
21. Ruiz-Sandoval JL, Cantu C, Barinagarrementeria F. Intracerebral hemorrhage in young people: analysis of risk factors, location, causes, and prognosis. Stroke; a journal of cerebral circulation. 1999; 30(3): 537-41. eng
22. Perret G, Nishioka H. Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section VI. Arteriovenous malformations. An analysis of 545 cases of cranio-cerebral arteriovenous malformations and fistulae reported to the cooperative study. J Neurosurg. 1966; 25(4): 467-90.
23. Yashar P, Amar AP, Giannotta SL, Yu C, Pagnini PG, Liu CY, et al. Cerebral arteriovenous malformations: issues of the interplay between stereotactic radiosurgery and endovascular surgical therapy. World neurosurgery. 2011; 75(5-6): 638-47. eng
24. HÖÖK O, Johanson C. Intracranial arteriovenous aneurysms: A follow-up study with particular attention to their growth. AMA Archives of Neurology & Psychiatry. 1958; 80(1): 39-54.
25. Ecker RD. Epistemology of Brain Arteriovenous Malformations. World neurosurgery. 2016; 89: 697-8.
26. Tong X, Wu J, Lin F, Cao Y, Zhao Y, Ning B, et al. The Effect of Age, Sex, and Lesion Location on Initial Presentation in Patients with Brain Arteriovenous Malformations. World neurosurgery. 2016; 87: 598-606.
27. Yang W, Caplan JM, Ye X, Wang JY, Braileanu M, Rigamonti D, et al. Racial Associations with Hemorrhagic Presentation in Cerebral Arteriovenous Malformations. World neurosurgery. 2015; 84(2): 461-9.
28. Choi EJ, Chen W, Jun K, Arthur HM, Young WL, Su H. Novel brain arteriovenous malformation mouse models for type 1 hereditary hemorrhagic telangiectasia. PLoS One. 2014; 9(2): e88511.
29. Nishida T, Faughnan ME, Krings T, Chakinala M, Gossage JR, Young WL, et al. Brain arteriovenous malformations associated with hereditary hemorrhagic telangiectasia: gene-phenotype correlations. Am J Med Genet A. 2012; 158A(11): 2829-34.
30. Letteboer TG, Mager JJ, Snijder RJ, Koeleman BP, Lindhout D, Ploos van Amstel JK, et al. Genotype-phenotype relationship in hereditary haemorrhagic telangiectasia. J Med Genet. 2006; 43(4): 371-7.
31. Matsubara S, Mandzia JL, ter Brugge K, Willinsky RA, Faughnan ME. Angiographic and clinical characteristics of patients with cerebral arteriovenous malformations associated with hereditary hemorrhagic telangiectasia. AJNR Am J Neuroradiol. 2000; 21(6): 1016-20.
32. Raj J, Stoodley M. Experimental Animal Models of Arteriovenous Malformation: A Review. Veterinary Sciences. 2015; 2(2): 97.
33. Willinsky RA, Lasjaunias P, Terbrugge K, Burrows P. Multiple cerebral arteriovenous malformations (AVMs). Review of our experience from 203 patients with cerebral vascular lesions. Neuroradiology. 1990; 32(3): 207-10.
34. Arthur HM, Ure J, Smith AJ, Renforth G, Wilson DI, Torsney E, et al. Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol. 2000; 217(1): 42-53.
35. Marchuk DA, Srinivasan S, Squire TL, Zawistowski JS. Vascular morphogenesis: tales of two syndromes. Hum Mol Genet. 2003; 12 Spec No 1: R97-112.
36. Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol. 2012; 13(10): 616-30.
37. Tual-Chalot S, Oh SP, Arthur HM. Mouse models of hereditary hemorrhagic telangiectasia: recent advances and future challenges. Front Genet. 2015; 6: 25.
38. March BT, Jayaraman MV. Aneurysms, arteriovenous malformations, and dural arteriovenous fistulas: diagnosis and treatment. Seminars in roentgenology. 2014; 49(1): 10-21. eng
39. Mouchtouris N, Jabbour PM, Starke RM, Hasan DM, Zanaty M, Theofanis T, et al. Biology of cerebral arteriovenous malformations with a focus on inflammation. J Cereb Blood Flow Metab. 2015; 35(2): 167-75.
40. Murphy PA, Kim TN, Huang L, Nielsen CM, Lawton MT, Adams RH, et al. Constitutively active Notch4 receptor elicits brain arteriovenous malformations through enlargement of capillary-like vessels. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111(50): 18007-12. eng
41. 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; a journal of cerebral circulation. 2009; 40(1): 100-5. eng
42. Novakovic RL, Lazzaro MA, Castonguay AC, Zaidat OO. The diagnosis and management of brain arteriovenous malformations. Neurol Clin. 2013; 31(3): 749-63.
43. Ajiboye N, Chalouhi N, Starke RM, Zanaty M, Bell R. Cerebral arteriovenous malformations: evaluation and management. ScientificWorldJournal. 2014; 2014: 649036.
44. Paramasivam S, Toma N, Niimi Y, Berenstein A. Development, clinical presentation and endovascular management of congenital intracranial pial arteriovenous fistulas. J Neurointerv Surg. 2013; 5(3): 184-90.
45. Robert T, Blanc R, Botta D, Ciccio G, Smajda S, Redjem H, et al. Management of multiple cerebral arteriovenous malformations in a non-pediatric population. Acta Neurochir (Wien). 2016.
46. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986; 65(4): 476-83.
47. Stapf C. The rationale behind "A Randomized Trial of Unruptured Brain AVMs" (ARUBA). Acta Neurochir Suppl. 2010; 107: 83-5.
48. Cenzato M, Delitala A, Delfini R, Pasqualin A, Maira G, Esposito V, et al. Position statement from the Italian Society of Neurosurgery on the ARUBA Study. J Neurosurg Sci. 2016; 60(1): 126-30.
49. Cockroft KM. Unruptured brain arteriovenous malformations should be treated conservatively: no. Stroke; a journal of cerebral circulation. 2007; 38(12): 3310-1. eng
50. Cockroft KM. Unruptured cerebral arteriovenous malformations: to treat or not to treat. Stroke; a journal of cerebral circulation. 2006; 37(5): 1148-9. eng
51. Schramm J, Schaller K, Esche J, Bostrom A. Microsurgery for cerebral arteriovenous malformations: subgroup outcomes in a consecutive series of 288 cases. J Neurosurg. 2016: 1-8.
52. Conger A, Kulwin C, Lawton MT, Cohen-Gadol AA. Diagnosis and evaluation of intracranial arteriovenous malformations. Surg Neurol Int. 2015; 6: 76.
53. Ledezma CJ, Hoh BL, Carter BS, Pryor JC, Putman CM, Ogilvy CS. Complications of cerebral arteriovenous malformation embolization: multivariate analysis of predictive factors. Neurosurgery. 2006; 58(4): 602-11; discussion -11.
54. Choudhri O, Ivan ME, Lawton MT. Transvenous Approach to Intracranial Arteriovenous Malformations: Challenging the Axioms of Arteriovenous Malformation Therapy? Neurosurgery. 2015; 77(4): 644-51; discussion 52.
55. Diaz O, Scranton R. Endovascular treatment of arteriovenous malformations. Handb Clin Neurol. 2016; 136: 1311-7.
56. Flickinger JC, Kondziolka D, Lunsford LD, Pollock BE, Yamamoto M, Gorman DA, et al. A multi-institutional analysis of complication outcomes after arteriovenous malformation radiosurgery. Int J Radiat Oncol Biol Phys. 1999; 44(1): 67-74.
57. Pradilla G, Coon AL, Huang J, Tamargo RJ. Surgical treatment of cranial arteriovenous malformations and dural arteriovenous fistulas. Neurosurgery clinics of North America. 2012; 23(1): 105-22.
58. Reitz M, von Spreckelsen N, Vettorazzi E, Burkhardt T, Grzyska U, Fiehler J, et al. Angioarchitectural Risk Factors for Hemorrhage and Clinical Long-Term Outcome in Pediatric Patients with Cerebral Arteriovenous Malformations. World neurosurgery. 2016; 89: 540-51.
59. Jabbour MN, Elder JB, Samuelson CG, Khashabi S, Hofman FM, Giannotta SL, et al. Aberrant angiogenic characteristics of human brain arteriovenous malformation endothelial cells. Neurosurgery. 2009; 64(1): 139-46; discussion 46-8.
60. Ferreira R, Santos T, Amar A, Tahara SM, Chen TC, Giannotta SL, et al. MicroRNA-18a improves human cerebral arteriovenous malformation endothelial cell function. Stroke; a journal of cerebral circulation. 2014; 45(1): 293-7.
61. Stapleton CJ, Armstrong DL, Zidovetzki R, Liu CY, Giannotta SL, Hofman FM. Thrombospondin-1 modulates the angiogenic phenotype of human cerebral arteriovenous malformation endothelial cells. Neurosurgery. 2011; 68(5): 1342-53; discussion 53. eng
62. Ferreira R, Santos T, Amar A, Gong A, Chen TC, Tahara SM, et al. Argonaute-2 promotes miR-18a entry in human brain endothelial cells. J Am Heart Assoc. 2014; 3(3): e000968.
63. Nijjar SS, Crosby HA, Wallace L, Hubscher SG, Strain AJ. Notch receptor expression in adult human liver: a possible role in bile duct formation and hepatic neovascularization. Hepatology. 2001; 34(6): 1184-92.
64. Tu J, Li Y, Hu Z. Notch1 and 4 signaling responds to an increasing vascular wall shear stress in a rat model of arteriovenous malformations. Biomed Res Int. 2014; 2014: 368082.
65. DiStefano PV, Kuebel JM, Sarelius IH, Glading AJ. KRIT1 protein depletion modifies endothelial cell behavior via increased vascular endothelial growth factor (VEGF) signaling. J Biol Chem. 2014; 289(47): 33054-65.
66. Yang IY, Yum MS, Kim EH, Choi HW, Yoo HW, Ko TS. Two cases of familial cerebral cavernous malformation caused by mutations in the CCM1 gene. Korean J Pediatr. 2016; 59(6): 280-4.
67. Boulday G, Rudini N, Maddaluno L, Blecon A, Arnould M, Gaudric A, et al. Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice. J Exp Med. 2011; 208(9): 1835-47.
68. Bravi L, Rudini N, Cuttano R, Giampietro C, Maddaluno L, Ferrarini L, et al. Sulindac metabolites decrease cerebrovascular malformations in CCM3-knockout mice. Proceedings of the National Academy of Sciences of the United States of America. 2015; 112(27): 8421-6.
69. He Y, Zhang H, Yu L, Gunel M, Boggon TJ, Chen H, et al. Stabilization of VEGFR2 signaling by cerebral cavernous malformation 3 is critical for vascular development. Sci Signal. 2010; 3(116): ra26.
70. Maddaluno L, Rudini N, Cuttano R, Bravi L, Giampietro C, Corada M, et al. EndMT contributes to the onset and progression of cerebral cavernous malformations. Nature. 2013; 498(7455): 492-6.
71. Bravi L, Malinverno M, Pisati F, Rudini N, Cuttano R, Pallini R, et al. Endothelial Cells Lining Sporadic Cerebral Cavernous Malformation Cavernomas Undergo Endothelial-to-Mesenchymal Transition. Stroke; a journal of cerebral circulation. 2016; 47(3): 886-90.
72. Bryan BA, D'Amore PA. What tangled webs they weave: Rho-GTPase control of angiogenesis. Cell Mol Life Sci. 2007; 64(16): 2053-65.
73. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010; 9(7): 689-701.
74. Borikova AL, Dibble CF, Sciaky N, Welch CM, Abell AN, Bencharit S, et al. Rho kinase inhibition rescues the endothelial cell cerebral cavernous malformation phenotype. J Biol Chem. 2010; 285(16): 11760-4.
75. Glading A, Han J, Stockton RA, Ginsberg MH. KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell cell junctions. J Cell Biol. 2007; 179(2): 247-54.
76. Stockton RA, Shenkar R, Awad IA, Ginsberg MH. Cerebral cavernous malformations proteins inhibit Rho kinase to stabilize vascular integrity. J Exp Med. 2010; 207(4): 881-96.
77. Whitehead KJ, Chan AC, Navankasattusas S, Koh W, London NR, Ling J, et al. The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases. Nat Med. 2009; 15(2): 177-84.
78. Zheng X, Xu C, Smith AO, Stratman AN, Zou Z, Kleaveland B, et al. Dynamic regulation of the cerebral cavernous malformation pathway controls vascular stability and growth. Dev Cell. 2012; 23(2): 342-55.
79. Zhou Z, Tang AT, Wong WY, Bamezai S, Goddard LM, Shenkar R, et al. Cerebral cavernous malformations arise from endothelial gain of MEKK3-KLF2/4 signalling. Nature. 2016; 532(7597): 122-6.
80. Geibprasert S, Pongpech S, Jiarakongmun P, Shroff MM, Armstrong DC, Krings T. Radiologic Assessment of Brain Arteriovenous Malformations: What Clinicians Need to Know. RadioGraphics. 2010; 30(2): 483-501.
81. Hernesniemi JA, Dashti R, Juvela S, Vaart K, Niemela 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): 823-9; discussion 9-31.
82. Lazar RM, Connaire K, Marshall RS, Pile-Spellman J, Hacein-Bey L, Solomon RA, et al. Developmental deficits in adult patients with arteriovenous malformations. Arch Neurol. 1999; 56(1): 103-6.
83. Hara H, Burrows PE, Flodmark O, Terbrugge K, Humphreys R. Neonatal superficial cerebral arteriovenous malformations. Pediatr Neurosurg. 1994; 20(2): 126-36.
84. Turjman F, Massoud TF, Sayre JW, Vinuela F, Guglielmi G, Duckwiler G. Epilepsy associated with cerebral arteriovenous malformations: a multivariate analysis of angioarchitectural characteristics. AJNR Am J Neuroradiol. 1995; 16(2): 345-50.
85. Darsaut TE, Magro E, Gentric JC, Batista AL, Chaalala C, Roberge D, et al. Treatment of Brain AVMs (TOBAS): study protocol for a pragmatic randomized controlled trial. Trials. 2015; 16: 497.
86. Sousa EC, Teixeira MJ, Piske RL, Albuquerque LS, Correa S, Benabou S, et al. The Role of Preradiosurgical Embolization in the Management of Grades III, IV, and V Arteriovenous Malformations. Front Surg. 2016; 3: 37.
87. Renieri L, Consoli A, Scarpini G, Grazzini G, Nappini S, Mangiafico S. Double arterial catheterization technique for embolization of brain arteriovenous malformations with onyx. Neurosurgery. 2013; 72(1): 92-8.
88. Lai LF, Chen JX, Zheng K, He XY, Li XF, Zhang X, et al. Posterior fossa brain arteriovenous malformations : Clinical features and outcomes of endovascular embolization, adjuvant microsurgery and radiosurgery. Clin Neuroradiol. 2016.
89. Huo X, Jiang Y, Lv X, Yang H, Zhao Y, Li Y. Gamma Knife surgical treatment for partially embolized cerebral arteriovenous malformations. J Neurosurg. 2016; 124(3): 767-76.
2. Brown RD, Jr., Wiebers DO, Forbes G, O'Fallon WM, Piepgras DG, Marsh WR, et al. The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg. 1988; 68(3): 352-7.
3. Zhao J, Wang S, Li J, Qi W, Sui D, Zhao Y. Clinical characteristics and surgical results of patients with cerebral arteriovenous malformations. Surgical neurology. 2005; 63(2): 156-61; discussion 61. eng
4. Martinez JL, Macdonald RL. Surgical Strategies for Acutely Ruptured Arteriovenous Malformations. Frontiers of neurology and neuroscience. 2015; 37: 166-81. eng
5. Murakami K, Endo T, Tominaga T. An analysis of flow dynamics in cerebral cavernous malformation and orbital cavernous angioma using indocyanine green videoangiography. Acta Neurochir (Wien). 2012; 154(7): 1169-75.
6. Gupta A, Periakaruppan A. Intracranial dural arteriovenous fistulas: A Review. Indian J Radiol Imaging. 2009; 19(1): 43-8.
7. Pabaney AH, Robin AM, Basheer A, Malik G. Surgical Management of Dural Arteriovenous Fistula After Craniotomy: Case Report and Review of Literature. World neurosurgery. 2016; 89: 731 e7- e11.
8. Lee JY, Son YJ, Kim JE. Intracranial pial arteriovenous fistulas. J Korean Neurosurg Soc. 2008; 44(2): 101-4.
9. Rohit, Goh PS. Diffuse Proliferative Cerebral Angiopathy: A case report and review of the literature. J Radiol Case Rep. 2015; 9(9): 1-10.
10. Guey S, Tournier-Lasserve E, Herve D, Kossorotoff M. Moyamoya disease and syndromes: from genetics to clinical management. Appl Clin Genet. 2015; 8: 49-68.
11. Pearl M, Gomez J, Gregg L, Gailloud P. Endovascular management of vein of Galen aneurysmal malformations. Influence of the normal venous drainage on the choice of a treatment strategy. Childs Nerv Syst. 2010; 26(10): 1367-79.
12. Berman MF, Sciacca RR, Pile-Spellman J, Stapf C, Connolly ES, Jr., Mohr JP, et al. The epidemiology of brain arteriovenous malformations. Neurosurgery. 2000; 47(2): 389-96; discussion 97.
13. Kim H, Su H, Weinsheimer S, Pawlikowska L, Young WL. Brain arteriovenous malformation pathogenesis: a response-to-injury paradigm. Acta Neurochir Suppl. 2011; 111: 83-92.
14. Carl J. Graf, George E. Perret, James C. Torner. Bleeding from cerebral arteriovenous malformations as part of their natural history. Journal of Neurosurgery. 1983; 58(3): 331-7.
15. Crawford PM, West CR, Chadwick DW, Shaw MD. Arteriovenous malformations of the brain: natural history in unoperated patients. J Neurol Neurosurg Psychiatry. 1986; 49(1): 1-10.
16. Forster DM, Steiner L, Hakanson S. Arteriovenous malformations of the brain. A long-term clinical study. J Neurosurg. 1972; 37(5): 562-70.
17. Mast H, Young WL, Koennecke HC, Sciacca RR, Osipov A, Pile-Spellman J, et al. Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation. Lancet. 1997; 350(9084): 1065-8.
18. Radvany MG, Gregg L. Endovascular treatment of cranial arteriovenous malformations and dural arteriovenous fistulas. Neurosurgery clinics of North America. 2012; 23(1): 123-31.
19. Stephen L. Ondra, Henry Troupp, Eugene D. George, Karen Schwab. The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. Journal of Neurosurgery. 1990; 73(3): 387-91.
20. Youichi Itoyama, Syouzaburou Uemura, Yukitaka Ushio, Jun-Ichi Kuratsu, Nobuhito Nonaka, Hidetaka Wada, et al. Natural course of unoperated intracranial arteriovenous malformations: study of 50 cases. Journal of Neurosurgery. 1989; 71(6): 805-9.
21. Ruiz-Sandoval JL, Cantu C, Barinagarrementeria F. Intracerebral hemorrhage in young people: analysis of risk factors, location, causes, and prognosis. Stroke; a journal of cerebral circulation. 1999; 30(3): 537-41. eng
22. Perret G, Nishioka H. Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section VI. Arteriovenous malformations. An analysis of 545 cases of cranio-cerebral arteriovenous malformations and fistulae reported to the cooperative study. J Neurosurg. 1966; 25(4): 467-90.
23. Yashar P, Amar AP, Giannotta SL, Yu C, Pagnini PG, Liu CY, et al. Cerebral arteriovenous malformations: issues of the interplay between stereotactic radiosurgery and endovascular surgical therapy. World neurosurgery. 2011; 75(5-6): 638-47. eng
24. HÖÖK O, Johanson C. Intracranial arteriovenous aneurysms: A follow-up study with particular attention to their growth. AMA Archives of Neurology & Psychiatry. 1958; 80(1): 39-54.
25. Ecker RD. Epistemology of Brain Arteriovenous Malformations. World neurosurgery. 2016; 89: 697-8.
26. Tong X, Wu J, Lin F, Cao Y, Zhao Y, Ning B, et al. The Effect of Age, Sex, and Lesion Location on Initial Presentation in Patients with Brain Arteriovenous Malformations. World neurosurgery. 2016; 87: 598-606.
27. Yang W, Caplan JM, Ye X, Wang JY, Braileanu M, Rigamonti D, et al. Racial Associations with Hemorrhagic Presentation in Cerebral Arteriovenous Malformations. World neurosurgery. 2015; 84(2): 461-9.
28. Choi EJ, Chen W, Jun K, Arthur HM, Young WL, Su H. Novel brain arteriovenous malformation mouse models for type 1 hereditary hemorrhagic telangiectasia. PLoS One. 2014; 9(2): e88511.
29. Nishida T, Faughnan ME, Krings T, Chakinala M, Gossage JR, Young WL, et al. Brain arteriovenous malformations associated with hereditary hemorrhagic telangiectasia: gene-phenotype correlations. Am J Med Genet A. 2012; 158A(11): 2829-34.
30. Letteboer TG, Mager JJ, Snijder RJ, Koeleman BP, Lindhout D, Ploos van Amstel JK, et al. Genotype-phenotype relationship in hereditary haemorrhagic telangiectasia. J Med Genet. 2006; 43(4): 371-7.
31. Matsubara S, Mandzia JL, ter Brugge K, Willinsky RA, Faughnan ME. Angiographic and clinical characteristics of patients with cerebral arteriovenous malformations associated with hereditary hemorrhagic telangiectasia. AJNR Am J Neuroradiol. 2000; 21(6): 1016-20.
32. Raj J, Stoodley M. Experimental Animal Models of Arteriovenous Malformation: A Review. Veterinary Sciences. 2015; 2(2): 97.
33. Willinsky RA, Lasjaunias P, Terbrugge K, Burrows P. Multiple cerebral arteriovenous malformations (AVMs). Review of our experience from 203 patients with cerebral vascular lesions. Neuroradiology. 1990; 32(3): 207-10.
34. Arthur HM, Ure J, Smith AJ, Renforth G, Wilson DI, Torsney E, et al. Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol. 2000; 217(1): 42-53.
35. Marchuk DA, Srinivasan S, Squire TL, Zawistowski JS. Vascular morphogenesis: tales of two syndromes. Hum Mol Genet. 2003; 12 Spec No 1: R97-112.
36. Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol. 2012; 13(10): 616-30.
37. Tual-Chalot S, Oh SP, Arthur HM. Mouse models of hereditary hemorrhagic telangiectasia: recent advances and future challenges. Front Genet. 2015; 6: 25.
38. March BT, Jayaraman MV. Aneurysms, arteriovenous malformations, and dural arteriovenous fistulas: diagnosis and treatment. Seminars in roentgenology. 2014; 49(1): 10-21. eng
39. Mouchtouris N, Jabbour PM, Starke RM, Hasan DM, Zanaty M, Theofanis T, et al. Biology of cerebral arteriovenous malformations with a focus on inflammation. J Cereb Blood Flow Metab. 2015; 35(2): 167-75.
40. Murphy PA, Kim TN, Huang L, Nielsen CM, Lawton MT, Adams RH, et al. Constitutively active Notch4 receptor elicits brain arteriovenous malformations through enlargement of capillary-like vessels. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111(50): 18007-12. eng
41. 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; a journal of cerebral circulation. 2009; 40(1): 100-5. eng
42. Novakovic RL, Lazzaro MA, Castonguay AC, Zaidat OO. The diagnosis and management of brain arteriovenous malformations. Neurol Clin. 2013; 31(3): 749-63.
43. Ajiboye N, Chalouhi N, Starke RM, Zanaty M, Bell R. Cerebral arteriovenous malformations: evaluation and management. ScientificWorldJournal. 2014; 2014: 649036.
44. Paramasivam S, Toma N, Niimi Y, Berenstein A. Development, clinical presentation and endovascular management of congenital intracranial pial arteriovenous fistulas. J Neurointerv Surg. 2013; 5(3): 184-90.
45. Robert T, Blanc R, Botta D, Ciccio G, Smajda S, Redjem H, et al. Management of multiple cerebral arteriovenous malformations in a non-pediatric population. Acta Neurochir (Wien). 2016.
46. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986; 65(4): 476-83.
47. Stapf C. The rationale behind "A Randomized Trial of Unruptured Brain AVMs" (ARUBA). Acta Neurochir Suppl. 2010; 107: 83-5.
48. Cenzato M, Delitala A, Delfini R, Pasqualin A, Maira G, Esposito V, et al. Position statement from the Italian Society of Neurosurgery on the ARUBA Study. J Neurosurg Sci. 2016; 60(1): 126-30.
49. Cockroft KM. Unruptured brain arteriovenous malformations should be treated conservatively: no. Stroke; a journal of cerebral circulation. 2007; 38(12): 3310-1. eng
50. Cockroft KM. Unruptured cerebral arteriovenous malformations: to treat or not to treat. Stroke; a journal of cerebral circulation. 2006; 37(5): 1148-9. eng
51. Schramm J, Schaller K, Esche J, Bostrom A. Microsurgery for cerebral arteriovenous malformations: subgroup outcomes in a consecutive series of 288 cases. J Neurosurg. 2016: 1-8.
52. Conger A, Kulwin C, Lawton MT, Cohen-Gadol AA. Diagnosis and evaluation of intracranial arteriovenous malformations. Surg Neurol Int. 2015; 6: 76.
53. Ledezma CJ, Hoh BL, Carter BS, Pryor JC, Putman CM, Ogilvy CS. Complications of cerebral arteriovenous malformation embolization: multivariate analysis of predictive factors. Neurosurgery. 2006; 58(4): 602-11; discussion -11.
54. Choudhri O, Ivan ME, Lawton MT. Transvenous Approach to Intracranial Arteriovenous Malformations: Challenging the Axioms of Arteriovenous Malformation Therapy? Neurosurgery. 2015; 77(4): 644-51; discussion 52.
55. Diaz O, Scranton R. Endovascular treatment of arteriovenous malformations. Handb Clin Neurol. 2016; 136: 1311-7.
56. Flickinger JC, Kondziolka D, Lunsford LD, Pollock BE, Yamamoto M, Gorman DA, et al. A multi-institutional analysis of complication outcomes after arteriovenous malformation radiosurgery. Int J Radiat Oncol Biol Phys. 1999; 44(1): 67-74.
57. Pradilla G, Coon AL, Huang J, Tamargo RJ. Surgical treatment of cranial arteriovenous malformations and dural arteriovenous fistulas. Neurosurgery clinics of North America. 2012; 23(1): 105-22.
58. Reitz M, von Spreckelsen N, Vettorazzi E, Burkhardt T, Grzyska U, Fiehler J, et al. Angioarchitectural Risk Factors for Hemorrhage and Clinical Long-Term Outcome in Pediatric Patients with Cerebral Arteriovenous Malformations. World neurosurgery. 2016; 89: 540-51.
59. Jabbour MN, Elder JB, Samuelson CG, Khashabi S, Hofman FM, Giannotta SL, et al. Aberrant angiogenic characteristics of human brain arteriovenous malformation endothelial cells. Neurosurgery. 2009; 64(1): 139-46; discussion 46-8.
60. Ferreira R, Santos T, Amar A, Tahara SM, Chen TC, Giannotta SL, et al. MicroRNA-18a improves human cerebral arteriovenous malformation endothelial cell function. Stroke; a journal of cerebral circulation. 2014; 45(1): 293-7.
61. Stapleton CJ, Armstrong DL, Zidovetzki R, Liu CY, Giannotta SL, Hofman FM. Thrombospondin-1 modulates the angiogenic phenotype of human cerebral arteriovenous malformation endothelial cells. Neurosurgery. 2011; 68(5): 1342-53; discussion 53. eng
62. Ferreira R, Santos T, Amar A, Gong A, Chen TC, Tahara SM, et al. Argonaute-2 promotes miR-18a entry in human brain endothelial cells. J Am Heart Assoc. 2014; 3(3): e000968.
63. Nijjar SS, Crosby HA, Wallace L, Hubscher SG, Strain AJ. Notch receptor expression in adult human liver: a possible role in bile duct formation and hepatic neovascularization. Hepatology. 2001; 34(6): 1184-92.
64. Tu J, Li Y, Hu Z. Notch1 and 4 signaling responds to an increasing vascular wall shear stress in a rat model of arteriovenous malformations. Biomed Res Int. 2014; 2014: 368082.
65. DiStefano PV, Kuebel JM, Sarelius IH, Glading AJ. KRIT1 protein depletion modifies endothelial cell behavior via increased vascular endothelial growth factor (VEGF) signaling. J Biol Chem. 2014; 289(47): 33054-65.
66. Yang IY, Yum MS, Kim EH, Choi HW, Yoo HW, Ko TS. Two cases of familial cerebral cavernous malformation caused by mutations in the CCM1 gene. Korean J Pediatr. 2016; 59(6): 280-4.
67. Boulday G, Rudini N, Maddaluno L, Blecon A, Arnould M, Gaudric A, et al. Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice. J Exp Med. 2011; 208(9): 1835-47.
68. Bravi L, Rudini N, Cuttano R, Giampietro C, Maddaluno L, Ferrarini L, et al. Sulindac metabolites decrease cerebrovascular malformations in CCM3-knockout mice. Proceedings of the National Academy of Sciences of the United States of America. 2015; 112(27): 8421-6.
69. He Y, Zhang H, Yu L, Gunel M, Boggon TJ, Chen H, et al. Stabilization of VEGFR2 signaling by cerebral cavernous malformation 3 is critical for vascular development. Sci Signal. 2010; 3(116): ra26.
70. Maddaluno L, Rudini N, Cuttano R, Bravi L, Giampietro C, Corada M, et al. EndMT contributes to the onset and progression of cerebral cavernous malformations. Nature. 2013; 498(7455): 492-6.
71. Bravi L, Malinverno M, Pisati F, Rudini N, Cuttano R, Pallini R, et al. Endothelial Cells Lining Sporadic Cerebral Cavernous Malformation Cavernomas Undergo Endothelial-to-Mesenchymal Transition. Stroke; a journal of cerebral circulation. 2016; 47(3): 886-90.
72. Bryan BA, D'Amore PA. What tangled webs they weave: Rho-GTPase control of angiogenesis. Cell Mol Life Sci. 2007; 64(16): 2053-65.
73. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010; 9(7): 689-701.
74. Borikova AL, Dibble CF, Sciaky N, Welch CM, Abell AN, Bencharit S, et al. Rho kinase inhibition rescues the endothelial cell cerebral cavernous malformation phenotype. J Biol Chem. 2010; 285(16): 11760-4.
75. Glading A, Han J, Stockton RA, Ginsberg MH. KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell cell junctions. J Cell Biol. 2007; 179(2): 247-54.
76. Stockton RA, Shenkar R, Awad IA, Ginsberg MH. Cerebral cavernous malformations proteins inhibit Rho kinase to stabilize vascular integrity. J Exp Med. 2010; 207(4): 881-96.
77. Whitehead KJ, Chan AC, Navankasattusas S, Koh W, London NR, Ling J, et al. The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases. Nat Med. 2009; 15(2): 177-84.
78. Zheng X, Xu C, Smith AO, Stratman AN, Zou Z, Kleaveland B, et al. Dynamic regulation of the cerebral cavernous malformation pathway controls vascular stability and growth. Dev Cell. 2012; 23(2): 342-55.
79. Zhou Z, Tang AT, Wong WY, Bamezai S, Goddard LM, Shenkar R, et al. Cerebral cavernous malformations arise from endothelial gain of MEKK3-KLF2/4 signalling. Nature. 2016; 532(7597): 122-6.
80. Geibprasert S, Pongpech S, Jiarakongmun P, Shroff MM, Armstrong DC, Krings T. Radiologic Assessment of Brain Arteriovenous Malformations: What Clinicians Need to Know. RadioGraphics. 2010; 30(2): 483-501.
81. Hernesniemi JA, Dashti R, Juvela S, Vaart K, Niemela 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): 823-9; discussion 9-31.
82. Lazar RM, Connaire K, Marshall RS, Pile-Spellman J, Hacein-Bey L, Solomon RA, et al. Developmental deficits in adult patients with arteriovenous malformations. Arch Neurol. 1999; 56(1): 103-6.
83. Hara H, Burrows PE, Flodmark O, Terbrugge K, Humphreys R. Neonatal superficial cerebral arteriovenous malformations. Pediatr Neurosurg. 1994; 20(2): 126-36.
84. Turjman F, Massoud TF, Sayre JW, Vinuela F, Guglielmi G, Duckwiler G. Epilepsy associated with cerebral arteriovenous malformations: a multivariate analysis of angioarchitectural characteristics. AJNR Am J Neuroradiol. 1995; 16(2): 345-50.
85. Darsaut TE, Magro E, Gentric JC, Batista AL, Chaalala C, Roberge D, et al. Treatment of Brain AVMs (TOBAS): study protocol for a pragmatic randomized controlled trial. Trials. 2015; 16: 497.
86. Sousa EC, Teixeira MJ, Piske RL, Albuquerque LS, Correa S, Benabou S, et al. The Role of Preradiosurgical Embolization in the Management of Grades III, IV, and V Arteriovenous Malformations. Front Surg. 2016; 3: 37.
87. Renieri L, Consoli A, Scarpini G, Grazzini G, Nappini S, Mangiafico S. Double arterial catheterization technique for embolization of brain arteriovenous malformations with onyx. Neurosurgery. 2013; 72(1): 92-8.
88. Lai LF, Chen JX, Zheng K, He XY, Li XF, Zhang X, et al. Posterior fossa brain arteriovenous malformations : Clinical features and outcomes of endovascular embolization, adjuvant microsurgery and radiosurgery. Clin Neuroradiol. 2016.
89. Huo X, Jiang Y, Lv X, Yang H, Zhao Y, Li Y. Gamma Knife surgical treatment for partially embolized cerebral arteriovenous malformations. J Neurosurg. 2016; 124(3): 767-76.
Published
2017-08-31
How to Cite
Eliahu, K., Hofman, F., & Giannotta, S. (2017). A Systematic Review of Cerebral Arteriovenous Malformation Management. International Journal of Medical Students, 5(2), 74–80. https://doi.org/10.5195/ijms.2017.13
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