Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-28T19:24:23.262Z Has data issue: false hasContentIssue false

Chapter 23 - Pediatric Vascular Malformations

from Section 2 - Clinical Neurosurgical Diseases

Published online by Cambridge University Press:  04 January 2024

By
Alaa Montaser  and
Edward R. Smith
Edited by
Farhana Akter ,
Nigel Emptage ,
Florian Engert  and
Mitchel S. Berger
Farhana Akter
Affiliation:
Harvard University, Massachusetts
Nigel Emptage
Affiliation:
University of Oxford
Florian Engert
Affiliation:
Harvard University, Massachusetts
Mitchel S. Berger
Affiliation:
University of California, San Francisco
Get access

Summary

Pediatric vascular malformations are a heterogeneous group of disorders that can generally be categorized into structural lesions and arteriopathies. The most common structural lesions encountered in pediatric neurosurgery include high-flow malformations involving abnormal connections between arteries and veins and low-flow malformations of aberrant capillary development(cavernous malformations). The term “moyamoya” is used to encompass a diverse group of arteriopathies characterized by the shared finding of progressive stenosis of the intracranial internal carotid arteries resulting in stroke. Here we will define these lesions, discuss epidemiology to put the scope of the disease in context, and then review the pathobiology in detail, with current genetic screening recommendations.

Type
Chapter
Information
Neuroscience for Neurosurgeons , pp. 314 - 325
Publisher: Cambridge University Press
Print publication year: 2024

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adil, MM, Qureshi, AI, Beslow, LA, Malik, AA, Jordan, LC. Factors associated with increased in-hospital mortality among children with intracerebral hemorrhage. J Child Neurol 2015;30(8):1024–8. https://doi.org/10.1177/0883073814552191.Google Scholar
Al-Jarallah, A, Al-Rifai, MT, Riela, AR, Roach, ES. Nontraumatic brain hemorrhage in children: etiology and presentation. J Child Neurol 2000;15:284–9. https://doi.org/10.1177/088307380001500503.Google Scholar
Al-Shahi, R, Bhattacharya, JJ, Currie, DG, et al. Prospective, population-based detection of intracranial vascular malformations in adults: the Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke 2003;34:1163–9. https://doi.org/10.1161/01.STR.0000069018.90456.C9.Google Scholar
Awad, IA, Polster, SP. Cavernous angiomas: deconstructing a neurosurgical disease. J Neurosurg 2019;131:1–13. https://doi.org/10.3171/2019.3.JNS181724.Google Scholar
Awad, IA, Robinson, JR, Jr., Mohanty, S, Estes, ML. Mixed vascular malformations of the brain: clinical and pathogenetic considerations. Neurosurgery 1993;33:179–88; discussion 88. https://doi.org/10.1227/00006123-199308000-00001.CrossRefGoogle ScholarPubMed
Bacigaluppi, S, Retta, SF, Pileggi, S, et al. Genetic and cellular basis of cerebral cavernous malformations: implications for clinical management. Clin Genet 2013;83:7–14. https://doi.org/10.1111/j.1399-0004.2012.01892.x.Google Scholar
Barnes, B, Cawley, CM, Barrow, DL. Intracerebral hemorrhage secondary to vascular lesions. Neurosurg Clin N Am 2002;13:289–97, v. https://doi.org/10.1016/s1042-3680(02)00015-3.Google Scholar
Baumgartner, JE, Ater, JL, Ha, CS, et al. Pathologically proven cavernous angiomas of the brain following radiation therapy for pediatric brain tumors. Pediatr Neurosurg 2003;39:201–07. https://doi.org/10.1159/000072472.Google Scholar
Beslow, LA, Licht, DJ, Smith, SE, et al. Predictors of outcome in childhood intracerebral hemorrhage: a prospective consecutive cohort study. Stroke 2010;41:313–8. https://doi.org/10.1161/STROKEAHA.109.568071.Google Scholar
Boon, LM, Mulliken, JB, Vikkula, M. RASA1: variable phenotype with capillary and arteriovenous malformations. Curr Opin Genet Dev 2005;15:265–9. https://doi.org/10.1016/j.gde.2005.03.004.Google Scholar
Bower, RS, Mallory, GW, Nwojo, M, Kudva, YC, Flemming, KD, Meyer, FB. Moyamoya disease in a primarily white, Midwestern US population: increased prevalence of autoimmune disease. Stroke 2013;44:1997–9. https://doi.org/10.1161/STROKEAHA.111.000307.Google Scholar
Broderick, J, Talbot, GT, Prenger, E, Leach, A, Brott, T. Stroke in children within a major metropolitan area: the surprising importance of intracerebral hemorrhage. J Child Neurol 1993;8:250–5. https://doi.org/10.1177/088307389300800308.CrossRefGoogle Scholar
Cavalcanti, DD, Kalani, MY, Martirosyan, NL, Eales, J, Spetzler, RF, Preul, MC. Cerebral cavernous malformations: from genes to proteins to disease. J Neurosurg 2012;116:122–32. https://doi.org/10.3171/2011.8.JNS101241.Google Scholar
Cecchi, AC, Guo, D, Ren, Z, et al. RNF213 rare variants in an ethnically diverse population with Moyamoya disease. Stroke 2014;45:3200–07. https://doi.org/10.1161/STROKEAHA.114.006244.Google Scholar
Chan, AC, Li, DY, Berg, MJ, Whitehead, KJ. Recent insights into cerebral cavernous malformations: animal models of CCM and the human phenotype. FEBS J 2010;277:1076–83. https://doi.org/10.1111/j.1742-4658.2009.07536.x.Google Scholar
Chee, D, Phillips, R, Maixner, W, Southwell, BR, Hutson, JM. The potential of capillary birthmarks as a significant marker for capillary malformation–arteriovenous malformation syndrome in children who had nontraumatic cerebral hemorrhage. J Pediatr Surg 2010;45:2419–22. https://doi.org/10.1016/j.jpedsurg.2010.08.043.Google Scholar
Chen, L, Tanriover, G, Yano, H, Friedlander, R, Louvi, A, Gunel, M. Apoptotic functions of PDCD10/CCM3, the gene mutated in cerebral cavernous malformation 3. Stroke 2009;40:1474–81. https://doi.org/10.1161/STROKEAHA.108.527135.CrossRefGoogle ScholarPubMed
Cooke, D, Tatum, J, Farid, H, Dowd, C, Higashida, R, Halbach, V. Transvenous embolization of a pediatric pial arteriovenous fistula. J Neurointerv Surg 2012;4:e14. https://doi.org/10.1136/neurintsurg-2011-010028.Google Scholar
Craig, HD, Gunel, M, Cepeda, O, et al. Multilocus linkage identifies two new loci for a mendelian form of stroke, cerebral cavernous malformation, at 7p15-13 and 3q25.2-27. Hum Mol Genet 1998;7:1851–8. https://doi.org/10.1093/hmg/7.12.1851.Google Scholar
Denier, C, Labauge, P, Bergametti, F, et al. Genotype–phenotype correlations in cerebral cavernous malformations patients. Ann Neurol 2006;60:550–6. https://doi.org/10.1002/ana.20947.Google Scholar
Di Rocco, C, Iannelli, A, Tamburrini, G. Cavernous angiomas of the brain stem in children. Pediatr Neurosurg 1997;27:92–9. https://doi.org/10.1159/000121233.Google Scholar
Dubovsky, J, Zabramski, JM, Kurth, J, et al. A gene responsible for cavernous malformations of the brain maps to chromosome 7q. Hum Mol Genet 1995;4:453–8. https://doi.org/10.1093/hmg/4.3.453.Google Scholar
Dupre, N, Verlaan, DJ, Hand, CK, et al. Linkage to the CCM2 locus and genetic heterogeneity in familial cerebral cavernous malformation. Can J Neurol Sci 2003;30:122–8. https://doi.org/10.1017/s0317167100053385.Google Scholar
Duran, D, Karschnia, P, Gaillard, JR, et al. Human genetics and molecular mechanisms of vein of Galen malformation. J Neurosurg Pediatr 2018;21:367–74. https://doi.org/10.3171/2017.9.PEDS17365.Google Scholar
Eerola, I, Boon, LM, Mulliken, JB, et al. Capillary malformation–arteriovenous malformation, a new clinical and genetic disorder caused by RASA1 mutations. Am J Hum Genet 2003;73:1240–9. https://doi.org/10.1086/379793.Google Scholar
Faughnan, ME, Palda, VA, Garcia-Tsao, G, et al. International guidelines for the diagnosis and management of hereditary haemorrhagic telangiectasia. J Med Genet 2011;48:73–87. https://doi.org/10.1136/jmg.2009.069013.CrossRefGoogle ScholarPubMed
Fehnel, KP, Penn, DL, Duggins-Warf, M, et al. Dysregulation of the EphrinB2–EphB4 ratio in pediatric cerebral arteriovenous malformations is associated with endothelial cell dysfunction in vitro and functions as a novel noninvasive biomarker in patients. Exp Mol Med 2020;52:658–71. https://doi.org/10.1038/s12276-020-0414-0.Google Scholar
Ferriero, DM, Fullerton, HJ, Bernard, TJ, et al. Management of stroke in neonates and children: a scientific statement from the American Heart Association/American Stroke Association. Stroke 2019;50:e51–e96. https://doi.org/10.1161/STR.0000000000000183.Google Scholar
Fish, JE, Flores-Suarez, CP, Boudreau, E, et al. Somatic gain of KRAS function in the endothelium is sufficient to cause vascular malformations that require MEK but not PI3K signaling. Circ Res 2020;127(6):727–43. https://doi.org/10.1161/CIRCRESAHA.CrossRefGoogle Scholar
Frim, DM, Scott, RM. Management of cavernous malformations in the pediatric population. Neurosurg Clin N Am 1999;10:513–8. https://doi.org/10.1016/S1042-3680(18)30182-7.Google Scholar
Fujimura, M, Watanabe, M, Narisawa, A, Shimizu, H, Tominaga, T. Increased expression of serum matrix metalloproteinase-9 in patients with moyamoya disease. Surg Neurol 2009;72:476–80; discussion 80. https://doi.org/10.1016/j.surneu.2008.10.009.Google Scholar
Fukui, M. Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (‘moyamoya’ disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan. Clin Neurol Neurosurg 1997;99(Suppl 2):S238–40.CrossRefGoogle ScholarPubMed
Fullerton, HJ, Wu, YW, Zhao, S, Johnston, SC. Risk of stroke in children: ethnic and gender disparities. Neurology 2003;61:189–94. https://doi.org/10.1212/01.wnl.0000078894.79866.95.Google Scholar
Gaillard, J, Klein, J, Duran, D, et al. Incidence, clinical features, and treatment of familial moyamoya in pediatric patients: a single-institution series. J Neurosurg Pediatr 2017;19:553–9. https://doi.org/10.3171/2016.12.PEDS16468.Google Scholar
Ganesan, V, Smith, ER. Moyamoya: defining current knowledge gaps. Dev Med Child Neurol 2015;57:786–7. https://doi.org/10.1111/dmcn.12708.Google Scholar
Garcia-Monaco, R, Taylor, W, Rodesch, G, et al. Pial arteriovenous fistula in children as presenting manifestation of Rendu–Osler–Weber disease. Neuroradiology 1995;37:60–4. https://doi.org/10.1007/BF00588522.CrossRefGoogle ScholarPubMed
Garrido-Martin, EM, Nguyen, HL, Cunningham, TA, et al. Common and distinctive pathogenetic features of arteriovenous malformations in hereditary hemorrhagic telangiectasia 1 and hereditary hemorrhagic telangiectasia 2 animal models – brief report. Arterioscler Thromb Vasc Biol 2014;34:2232–6. https://doi.org/10.1161/ATVBAHA.114.303984.Google Scholar
Gauden, AJ, McRobb, LS, Lee, VS, et al. Occlusion of animal model arteriovenous malformations using vascular targeting. Transl Stroke Res 2020;11:689–99. https://doi.org/10.1007/s12975-019-00759-y.CrossRefGoogle ScholarPubMed
Gault, J, Sarin, H, Awadallah, NA, Shenkar, R, Awad, IA. Pathobiology of human cerebrovascular malformations: basic mechanisms and clinical relevance. Neurosurgery 2004;55:1–16; discussion 16–7. https://doi.org/10.1227/01.neu.0000440729.59133.c9.Google Scholar
Gil-Nagel, A, Dubovsky, J, Wilcox, KJ, et al. Familial cerebral cavernous angioma: a gene localized to a 15-cM interval on chromosome 7q. Ann Neurol 1996;39:807–10. https://doi.org/10.1002/ana.410390619.Google Scholar
Goss, JA, Huang, AY, Smith, E, et al. Somatic mutations in intracranial arteriovenous malformations. PLoS One 2019;14:e0226852. https://doi.org/10.1371/journal.pone.0226852.Google Scholar
Gross, BA, Du, R, Orbach, DB, Scott, RM, Smith, ER. The natural history of cerebral cavernous malformations in children. J Neurosurg Pediatr 2016;17(2):123–8. https://doi.org/10.3171/2015.2.PEDS14541.Google Scholar
Gross, BA, Smith, ER, Goumnerova, L, Proctor, MR, Madsen, JR, Scott, RM. Resection of supratentorial lobar cavernous malformations in children: clinical article. J Neurosurg Pediatr 2013a;12:367–73. https://doi.org/10.3171/2013.7.PEDS13126.Google Scholar
Gross, BA, Smith, ER, Scott, RM. Cavernous malformations of the basal ganglia in children. J Neurosurg Pediatr 2013b;12:171–4. https://doi.org/10.3171/2013.5.PEDS1335.CrossRefGoogle ScholarPubMed
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. https://doi.org/10.2147/TACG.S42772.Google Scholar
Gunel, M, Awad, IA, Anson, J, Lifton, RP. Mapping a gene causing cerebral cavernous malformation to 7q11.2-q21. Proc Natl Acad Sci U S A 1995;92:6620–4. https://doi.org/10.1073/pnas.92.14.6620.Google Scholar
Gunel, M, Awad, IA, Finberg, K, et al. A founder mutation as a cause of cerebral cavernous malformation in Hispanic Americans. N Engl J Med 1996;334:946–51. https://doi.org/10.1056/NEJM199604113341503.Google Scholar
Hang, Z, Shi, Y, Wei, Y. [A pathological analysis of 180 cases of vascular malformation of brain]. Zhonghua Bing Li Xue Za Zhi 1996;25:135–8.Google Scholar
Hayman, LA, Evans, RA, Ferrell, RE, Fahr, LM, Ostrow, P, Riccardi, VM. Familial cavernous angiomas: natural history and genetic study over a 5-year period. Am J Med Genet 1982;11:147–60. https://doi.org/10.1002/ajmg.1320110205.Google Scholar
Hetts, SW, Keenan, K, Fullerton, HJ, et al. Pediatric intracranial nongalenic pial arteriovenous fistulas: clinical features, angioarchitecture, and outcomes. Am J Neuroradiol 2012;33:1710–9. https://doi.org/10.3174/ajnr.A3194.CrossRefGoogle ScholarPubMed
Hyacinth, HI, Sugihara, CL, Spencer, TL, Archer, DR, Shih, AY. Higher prevalence of spontaneous cerebral vasculopathy and cerebral infarcts in a mouse model of sickle cell disease. J Cereb Blood Flow Metab 2019;39:342–51. https://doi.org/10.1177/0271678X17732275.Google Scholar
Jia, L, Wang, L, Wei, F, et al. Effects of wall shear stress in venous neointimal hyperplasia of arteriovenous fistulae. Nephrology (Carlton) 2015;20:335–42. https://doi.org/10.1111/nep.12394.Google Scholar
Jordan, LC, Kleinman, JT, Hillis, AE. Intracerebral hemorrhage volume predicts poor neurologic outcome in children. Stroke 2009;40:1666–71. https://doi.org/10.1161/STROKEAHA.108.541383.Google Scholar
Kang, HS, Kim, JH, Phi, JH, et al. Plasma matrix metalloproteinases, cytokines and angiogenic factors in moyamoya disease. J Neurol Neurosurg Psychiatry 2010;81:673–8. https://doi.org/10.1136/jnnp.2009.191817.CrossRefGoogle ScholarPubMed
Kim, J. Introduction to cerebral cavernous malformation: a brief review. BMB Rep 2016;49:255–62. https://doi.org/10.5483/bmbrep.2016.49.5.036.Google Scholar
Kim, YH, Choe, SW, Chae, MY, Hong, S, Oh, SP. SMAD4 deficiency leads to development of arteriovenous malformations in neonatal and adult mice. J Am Heart Assoc 2018;7:e009514. https://doi.org/10.1161/JAHA.118.009514.Google Scholar
Kurek, KC, Luks, VL, Ayturk, UM, et al. Somatic mosaic activating mutations in PIK3CA cause CLOVES syndrome. Am J Hum Genet 2012;90:1108–15. https://doi.org/10.1016/j.ajhg.2012.05.006.Google Scholar
Labauge, P, Enjolras, O, Bonerandi, JJ, et al. An association between autosomal dominant cerebral cavernomas and a distinctive hyperkeratotic cutaneous vascular malformation in 4 families. Ann Neurol 1999;45:250–4. https://doi.org/10.1002/1531-8249(199902)45:2<250::aid-ana17>3.0.co;2-v.Google Scholar
Laberge, S, Labauge, P, Marechal, E, Maciazek, J, Tournier-Lasserve, E. Genetic heterogeneity and absence of founder effect in a series of 36 French cerebral cavernous angiomas families. Eur J Hum Genet 1999;7:499–504. https://doi.org/10.1038/sj.ejhg.5200324.Google Scholar
Laberge-le Couteulx, S, Jung, HH, Labauge, P, et al. Truncating mutations in CCM1, encoding KRIT1, cause hereditary cavernous angiomas. Nat Genet 1999;23:189–93. https://doi.org/10.1038/13815.Google Scholar
Larson, JJ, Ball, WS, Bove, KE, Crone, KR, Tew, JM, Jr. Formation of intracerebral cavernous malformations after radiation treatment for central nervous system neoplasia in children. J Neurosurg 1998;88:51–6. https://doi.org/10.3171/jns.1998.88.1.0051.Google Scholar
Lasjaunias, P. Vascular Diseases in Neonates, Infants and Children. Springer Verlag; 1997.Google Scholar
Laurans, MS, DiLuna, ML, Shin, D, et al. Mutational analysis of 206 families with cavernous malformations. J Neurosurg 2003;99:38–43. https://doi.org/10.3171/jns.2003.99.1.0038.Google Scholar
Lawton, MT, Rutledge, WC, Kim, H, et al. Brain arteriovenous malformations. Nat Rev Dis Primers 2015;1:15008. https://doi.org/10.1038/nrdp.2015.8.Google Scholar
Lee, MJ, Chen, YF, Fan, PC, et al. Mutation genotypes of RNF213 gene from moyamoya patients in Taiwan. J Neurol Sci 2015;353:161–5. https://doi.org/10.1016/j.jns.2015.04.019.Google Scholar
Liu, J, Wang, D, Lei, C, et al. Etiology, clinical characteristics and prognosis of spontaneous intracerebral hemorrhage in children: a prospective cohort study in China. J Neurol Sci 2015;358:367–70. https://doi.org/10.1016/j.jns.2015.09.366.Google Scholar
Mansour, A, Niizuma, K, Rashad, S, et al. A refined model of chronic cerebral hypoperfusion resulting in cognitive impairment and a low mortality rate in rats. J Neurosurg 2018;131:892–902. https://doi.org/10.3171/2018.3.JNS172274.Google Scholar
Marchuk, DA, Gallione, CJ, Morrison, LA, et al. A locus for cerebral cavernous malformations maps to chromosome 7q in two families. Genomics 1995;28:311–4. https://doi.org/10.1006/geno.1995.1147.Google Scholar
Matsuda, Y, Mineharu, Y, Kimura, M, et al. RNF213 p.R4810K variant and intracranial arterial stenosis or occlusion in relatives of patients with moyamoya disease. J Stroke Cerebrovasc Dis 2017;26:1841–7. https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.04.019.CrossRefGoogle ScholarPubMed
Merello, E, Pavanello, M, Consales, A, et al. Genetic screening of pediatric cavernous malformations. J Mol Neurosci 2016;60:232–8. https://doi.org/10.1007/s12031-016-0806-8.Google Scholar
Miskinyte, S, Butler, MG, Herve, D, et al. Loss of BRCC3 deubiquitinating enzyme leads to abnormal angiogenesis and is associated with syndromic moyamoya. Am J Hum Genet 2011;88:718–28. https://doi.org/10.1016/j.ajhg.2011.04.017.Google Scholar
Mohr, JP, Parides, MK, Stapf, C, et al. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 2014;383:614–21. https://doi.org/10.1016/S0140-6736(13)62302-8.Google Scholar
Mottolese, C, Hermier, M, Stan, H, et al. Central nervous system cavernomas in the pediatric age group. Neurosurg Rev 2001;24:55–71; discussion 2–3. https://doi.org/10.1007/pl00014581.Google Scholar
Munot, P, Saunders, DE, Milewicz, DM, et al. A novel distinctive cerebrovascular phenotype is associated with heterozygous Arg179 ACTA2 mutations. Brain 2012;135:2506–14. https://doi.org/10.1093/brain/aws172.Google Scholar
Pinard, A, Guey, S, Guo, D, et al. The pleiotropy associated with de novo variants in CHD4, CNOT3, and SETD5 extends to moyamoya angiopathy. Genet Med 2020;22:427–31. https://doi.org/10.1038/s41436-019-0639-2.Google Scholar
Pricola Fehnel, K, Duggins-Warf, M, Zurakowski, D, et al. Using urinary bFGF and TIMP3 levels to predict the presence of juvenile pilocytic astrocytoma and establish a distinct biomarker signature. J Neurosurg Pediatr 2016;18:396–407. https://doi.org/10.3171/2015.12.PEDS15448.Google Scholar
Protack, CD, Foster, TR, Hashimoto, T, et al. Eph-B4 regulates adaptive venous remodeling to improve arteriovenous fistula patency. Sci Rep 2017;7:15386. https://doi.org/10.1038/s41598-017-13071-2.Google Scholar
Raj, JA, Stoodley, M. Experimental animal models of arteriovenous malformation: a review. Vet Sci 2015;2:97–110. https://doi.org/10.3390/vetsci2020097.Google Scholar
Raybaud, CA, Strother, CM, Hald, JK. Aneurysms of the vein of Galen: embryonic considerations and anatomical features relating to the pathogenesis of the malformation. Neuroradiology 1989;31:109–28. https://doi.org/10.1007/BF00698838.Google Scholar
Recinos, PF, Rahmathulla, G, Pearl, M, et al. Vein of Galen malformations: epidemiology, clinical presentations, management. Neurosurg Clin N Am 2012;23:165–77. https://doi.org/10.1016/j.nec.2011.09.006.Google Scholar
Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis, and Health Labour Sciences Research Grant for Research on Measures for Infractable Diseases. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 2012;52:245–66. https://doi.org/10.2176/nmc.52.245.Google Scholar
Rigamonti, D, Hadley, MN, Drayer, BP, et al. Cerebral cavernous malformations. Incidence and familial occurrence. N Engl J Med 1988;319:343–7. https://doi.org/10.1056/NEJM198808113190605.Google Scholar
Riordan, CP, Orbach, DB, Smith, ER, Scott, RM. Acute fatal hemorrhage from previously undiagnosed cerebral arteriovenous malformations in children: a single-center experience. J Neurosurg Pediatr 2018;22:244–50. https://doi.org/10.3171/2018.3.PEDS1825.Google Scholar
Roberts, JM, Maniskas, ME, Fraser, JF, Bix, GJ. Internal carotid artery stenosis: a novel surgical model for moyamoya syndrome. PLoS One 2018;13:e0191312. https://doi.org/10.1371/journal.pone.0191312Google Scholar
Rutledge, WC, Abla, AA, Nelson, J, Halbach, VV, Kim, H, Lawton, MT. Treatment and outcomes of ARUBA-eligible patients with unruptured brain arteriovenous malformations at a single institution. Neurosurg Focus 2014;37:E8. https://doi.org/10.3171/2014.7.FOCUS14242.Google Scholar
Saliou, G, Eyries, M, Iacobucci, M, et al. Clinical and genetic findings in children with CNS arteriovenous fistulas. Ann Neurol 2017;82(6):972–80. https://doi.org/10.1002/ana.25106.Google Scholar
Scott, RM. Brain stem cavernous angiomas in children. Pediatr Neurosurg 1990;16:281–6. https://doi.org/10.1159/000120543.Google Scholar
Scott, RM, Barnes, P, Kupsky, W, Adelman, LS. Cavernous angiomas of the central nervous system in children. J Neurosurg 1992;76:38–46. https://doi.org/10.3171/jns.1992.76.1.0038.Google Scholar
Scott, RM, Smith, ER. Moyamoya disease and moyamoya syndrome. N Engl J Med 2009;360:1226–37. https://doi.org/10.1056/NEJMra0804622.Google Scholar
Seki, T, Yun, J, Oh, SP. Arterial endothelium-specific activin receptor-like kinase 1 expression suggests its role in arterialization and vascular remodeling. Circ Res 2003;93:682–9. https://doi.org/10.1161/01.RES.0000095246.40391.3B.Google Scholar
Shenkar, R, Elliott, JP, Diener, K, et al. Differential gene expression in human cerebrovascular malformations. Neurosurgery 2003;52:465–77; discussion 77–8. https://doi.org/10.1227/01.neu.0000044131.03495.22.Google Scholar
Singla, A, Brace O’Neill, JE, Smith, E, Scott, RM. Cavernous malformations of the brain after treatment for acute lymphocytic leukemia: presentation and long-term follow-up. J Neurosurg Pediatr 2013;11:127–32. https://doi.org/10.3171/2012.11.PEDS12235.Google Scholar
Sirvente, J, Enjolras, O, Wassef, M, Tournier-Lasserve, E, Labauge, P. Frequency and phenotypes of cutaneous vascular malformations in a consecutive series of 417 patients with familial cerebral cavernous malformations. J Eur Acad Dermatol Venereol 2009;23(9):1066–72. https://www/doi/10.1111/j.1468-3083.2009.03263.x.Google Scholar
Smith, ER. Moyamoya biomarkers. J Korean Neurosurg Soc 2015;57:415–21. https://doi.org/10.3340/jkns.2015.57.6.415.Google Scholar
Smith, ER, Scott, RM. Spontaneous occlusion of the circle of Willis in children: pediatric moyamoya summary with proposed evidence-based practice guidelines. A review. J Neurosurg Pediatr 2012;9:353–60. https://doi.org/10.3171/2011.12.PEDS1172.CrossRefGoogle ScholarPubMed
Somarathna, M, Isayeva-Waldrop, T, Al-Balas, A, Guo, L, Lee, T. Novel, A Model of balloon angioplasty injury in rat arteriovenous fistula. J Vasc Res 2020;57(4):223–35. https://doi.org/10.1159/000507080.Google Scholar
Soriano, SG, Cowan, DB, Proctor, MR, Scott, RM. Levels of soluble adhesion molecules are elevated in the cerebrospinal fluid of children with moyamoya syndrome. Neurosurgery 2002;50:544–9. https://doi.org/10.1097/00006123-200203000-00022.Google Scholar
Spiegler, S, Rath, M, Paperlein, C, Felbor, U. Cerebral cavernous malformations: an update on prevalence, molecular genetic analyses, and genetic counselling. Mol Syndromol 2018;9:60–9. https://doi.org/10.1159/000486292.Google Scholar
Starke, RM, McCarthy, DJ, Komotar, RJ, Connolly, ES. Gut microbiome and endothelial TLR4 activation provoke cerebral cavernous malformations. Neurosurgery 2017;81:N44–N6. https://doi.org/10.1093/neuros/nyx450.Google Scholar
Tang, AT, Choi, JP, Kotzin, JJ, et al. Endothelial TLR4 and the microbiome drive cerebral cavernous malformations. Nature 2017;545:305–10. https://doi.org/10.1038/nature22075.Google Scholar
Tanriover, G, Boylan, AJ, Diluna, ML, Pricola, KL, Louvi, A, Gunel, M. PDCD10, the gene mutated in cerebral cavernous malformation 3, is expressed in the neurovascular unit. Neurosurgery 2008;62:930–8; discussion 8. https://doi.org/10.1227/01.neu.0000318179.02912.ca.Google Scholar
Thiex, R, Mulliken, JB, Revencu, N, et al. A novel association between RASA1 mutations and spinal arteriovenous anomalies.Am J Neuroradiol 2010;31:775–9. https://doi.org/10.3174/ajnr.A1907.Google Scholar
Toll, A, Parera, E, Gimenez-Arnau, AM, et al. Cutaneous venous malformations in familial cerebral cavernomatosis caused by KRIT1 gene mutations. Dermatology 2009;218:307–13. https://doi.org/10.1159/000199461.Google Scholar
Tomlinson, FH, Rufenacht, DA, Sundt, TM, Jr., Nichols, DA, Fode, NC. Arteriovenous fistulas of the brain and the spinal cord. J Neurosurg 1993;79:16–27. https://doi.org/10.3171/jns.1993.79.1.0016Google Scholar
Vanaman, MJ, Hervey-Jumper, SL, Maher, CO. Pediatric and inherited neurovascular diseases. Neurosurg Clin N Am 2010;21:427–41. https://doi.org/10.1016/j.nec.2010.03.001.Google Scholar
Vivanti, A, Ozanne, A, Grondin, C, et al. Loss of function mutations in EPHB4 are responsible for vein of Galen aneurysmal malformation. Brain 2018;141:979–88. https://doi.org/10.1093/brain/awy020.Google Scholar
Walcott, BP, Smith, ER, Scott, RM, Orbach, DB. Dural arteriovenous fistulae in pediatric patients: associated conditions and treatment outcomes. J Neurointerv Surg 2013a;5(1):6–9. https://doi.org/10.1136/neurintsurg-2011-010169.Google Scholar
Walcott, BP, Smith, ER, Scott, RM, Orbach, DB. Pial arteriovenous fistulae in pediatric patients: associated syndromes and treatment outcome. J Neurointerv Surg 2013b;5(1):10–4. https://doi.org/10.1136/neurintsurg-2011-010168.Google ScholarPubMed
Wallace, S, Guo, DC, Regalado, E, et al. Disrupted nitric oxide signaling due to GUCY1A3 mutations increases risk for moyamoya disease, achalasia and hypertension. Clin Genet 2016;90:351–60. https://doi.org/10.1111/cge.12739.CrossRefGoogle ScholarPubMed
Wang, K, Zhou, HJ, Wang, M. CCM3 and cerebral cavernous malformation disease. Stroke Vasc Neurol 2019;4:67–70. https://doi.org/10.1136/svn-2018-000195.Google Scholar
Warejko, JK, Schueler, M, Vivante, A, et al. Whole exome sequencing reveals a monogenic cause of disease in approximately 43% of 35 families with midaortic syndrome. Hypertension 2018;71:691–9. https://doi.org/10.1161/HYPERTENSIONAHA.117.10296.Google Scholar
Wen, J, Sun, X, Chen, H, et al. Mutation of rnf213a by TALEN causes abnormal angiogenesis and circulation defects in zebrafish. Brain Res 2016;1644:70–8. https://doi.org/10.1016/j.brainres.2016.04.051.CrossRefGoogle ScholarPubMed
Weon, YC, Yoshida, Y, Sachet, M, et al. Supratentorial cerebral arteriovenous fistulas (AVFs) in children: review of 41 cases with 63 non choroidal single-hole AVFs. Acta Neurochir (Wien) 2005;147:17–31. https://doi.org/10.1007/s00701-004-0341-1.Google Scholar
Wetzel-Strong, SE, Detter, MR, Marchuk, DA. The pathobiology of vascular malformations: insights from human and model organism genetics. J Pathol 2017;241:281–93. https://doi.org/10.1002/path.4844.Google Scholar
Whitehead, KJ, Plummer, NW, Adams, JA, Marchuk, DA, Li, DY. Ccm1 is required for arterial morphogenesis: implications for the etiology of human cavernous malformations. Development 2004;131:1437–48. https://doi.org/10.1242/dev.01036.Google Scholar
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;32:207–10. https://doi.org/10.1007/BF00589113.Google Scholar
Woodall, MN, McGettigan, M, Figueroa, R, Gossage, JR, Alleyne, CH, Jr. Cerebral vascular malformations in hereditary hemorrhagic telangiectasia. J Neurosurg 2014;120:87–92. https://doi.org/10.3171/2013.10.JNS122402.Google Scholar
Yoshida, Y, Weon, YC, Sachet, M, et al. Posterior cranial fossa single-hole arteriovenous fistulae in children: 14 consecutive cases. Neuroradiology 2004;46:474–81. https://doi.org/10.1007/s00234-004-1176-4.Google Scholar
Zabramski, JM, Wascher, TM, Spetzler, RF, et al. The natural history of familial cavernous malformations: results of an ongoing study. J Neurosurg 1994;80:422–32. https://doi.org/10.3171/jns.1994.80.3.0422.Google Scholar
Zeng, X, Hunt, A, Jin, SC, Duran, D, Gaillard, J, Kahle, KT. EphrinB2–EphB4–RASA1 signaling in human cerebrovascular development and disease. Trends Mol Med 2019;25:265–86. https://doi.org/10.1016/j.molmed.2019.01.009.Google Scholar
Zhang, J, Rigamonti, D, Dietz, HC, Clatterbuck, RE. Interaction between krit1 and malcavernin: implications for the pathogenesis of cerebral cavernous malformations. Neurosurgery 2007;60:353–9; discussion 9. https://doi.org/10.1227/01.NEU.0000249268.11074.83.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×