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Cavernomas

  • Luca MassimiEmail author
  • Souvik Kar
  • Mario Giordano
  • Helmut Bertalanffy
Living reference work entry

Abstract

Cerebral cavernous malformations (CMs) have since long time been recognized as one of the most common vascular malformations of the central nervous system together with arteriovenous malformations, capillary telangiectasias, and venous angiomas. CMs were also described as occult vascular malformations because no abnormal vascularity is seen on angiography due to the absence of direct arterial input (Attar et al. 2001). The term “cavernous angioma” was first used by Russell and Rubinstein in their description of the pathology of brain lesions (Russell and Rubinstein 1989). CMs are also known as cavernous hemangioma, cavernous venous malformation, or simply cavernoma. The term “cavernous malformation” or “cavernoma” is usually preferred to the term “cavernous angioma” to distinguish CMs from the shunting-associated malformations or the vascular neoplasms (Patel et al. 2012).

References

  1. Acciarri N, Galassi E, Giulioni M, Pozzati E, Grasso V, Palandri G, Badaloni F, Zucchelli M, Calbucci F (2009) Cavernous malformations of the central nervous system in the pediatric age group. Pediatr Neurosurg 45:81–104PubMedCrossRefGoogle Scholar
  2. Aiba T, Tanaka R, Koike T, Kameyama S, Takeda N, Komata T (1995) Natural history of intracranial cavernous malformations. J Neurosurg 83:56–59PubMedCrossRefGoogle Scholar
  3. Alexiou GA, Mpairamidis E, Sfakianos G, Prodromou N (2009) Surgical management of brain cavernomas in children. Pediatr Neurosurg 45:375–378PubMedCrossRefGoogle Scholar
  4. Al-Holou WN, O’Lynnger TM, Pandey AS, Gemmete JJ, Thompson BG, Muraszko KM, Garton HJ, Maher CO (2012) Natural history and imaging prevalence of cavernous malformations in children and young adults. J Neurosurg Pediatr 9:198–205PubMedCrossRefGoogle Scholar
  5. Amato MC, Madureira JF, Oliveira RS (2013) Intracranial cavernous malformation in children: a single-centered experience with 30 consecutive cases. Arq Neuropsiquiatr 71:220–228PubMedCrossRefGoogle Scholar
  6. Attar A, Ugur HC, Savas A, Yuceer N, Egemen N (2001) Surgical treatment of intracranial cavernous angiomas. J Clin Neurosci 8:235–239PubMedCrossRefGoogle Scholar
  7. Batra S, Crain B, Engelmann R, Camara-Quintana J, Rigamonti D (2011) Pathology of cavernous malformations. In: Rigamonti D (ed) Cavernous malformations of the nervous system. Cambridge University Press, Cambridge, pp 1–7Google Scholar
  8. Baumann CR, Schuknecht B, Lo Russo G, Cossu M, Citterio A, Andermann F, Siegel AM (2006) Seizure outcome after resection of cavernous malformations is better when surrounding hemosiderin-stained brain also is removed. Epilepsia 47:563–566PubMedCrossRefGoogle Scholar
  9. Baumann CR, Acciarri N, Bertalanffy H, Devinsky O, Elger CE, Lo Russo G, Cossu M, Sure U, Singh A, Stefan H, Hammen T, Georgiadis D, Baumgartner RW, Andermann F, Siegel AM (2007) Seizure outcome after resection of supratentorial cavernous malformations: a study of 168 patients. Epilepsia 48:559–563PubMedCrossRefGoogle Scholar
  10. Bertalanffy H, Gerganov VM (2013) Microsurgical or radiosurgical management of intracranial cavernomas. Acta Neurochir Suppl 116:103–106PubMedGoogle Scholar
  11. Bertalanffy H, Benes L, Miyazawa T, Alberti O, Siegel AM, Sure U (2002) Cerebral cavernomas in the adult. Review of the literature and analysis of 72 surgically treated patients. Neurosurg Rev 25:1–53PubMedCrossRefGoogle Scholar
  12. Bertalanffy H, Burkhardt JK, Alfons Kockro R, Bozinov O, Sarnthein J (2011) Resection of cavernous malformations of the brainstem. In: Rigamonti D (ed) Cavernous malformations of the nervous system. Cambridge University Press, Cambridge, pp 142–160Google Scholar
  13. Bertalanffy H, Gerganov V, Paterno V (in press) Surgical management of supratentorial cavernous malformations. In: Spetzler R et al (eds) Neurovascular Surgery. Thieme Medical Publishers, New York, pp 419–435Google Scholar
  14. Berti I, Marchetti F, Skabar A, Zennaro F, Zanon D, Ventura A (2014) Propranolol for cerebral cavernous angiomatosis: a magic bullet. Clin Pediatr (Phila) 53:189–190CrossRefGoogle Scholar
  15. Bozinov O, Hatano T, Sarntheina J, Burkhardta JK, Bertalanffy H (2010) Current clinical management of brainstem cavernomas. Swiss Med Wkly 140:w13120PubMedGoogle Scholar
  16. Cavalcanti DD, Preul MC, Kalani MYS, Spetzler RF (2016) Microsurgical anatomy of safe entry zones to the brainstem. J Neurosurg 124:1359–1376PubMedCrossRefGoogle Scholar
  17. Cenzato M, Stefini R, Ambrosi C, Giovanelli M (2008) Post-operative remnants of brainstem cavernomas: incidence, risk factors and management. Acta Neurochir 150:879–886PubMedCrossRefGoogle Scholar
  18. Chang EF, Gabriel RA, Potts MB, Garcia PA, Barbaro NM, Lawton MT (2009) Seizure characteristics and control after microsurgical resection of supratentorial cerebral cavernous malformations. Neurosurgery 65:31–37PubMedCrossRefGoogle Scholar
  19. Cigoli MS, Avemaria F, De Benedetti S, Gesu GP, Accorsi LG, Parmigiani S, Corona MF, Capra V, Mosca A, Giovannini S, Notturno F, Ciccocioppo F, Volpi L, Estienne M, De Michele G, Antenora A, Bilo L, Tavoni A, Zamponi N, Alfei E, Baranello G, Riva D, Penco S (2014) PDCD10 gene mutations in multiple cerebral cavernous malformations. PLoS One 9:e110438PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cohen DS, Zubay GP, Goodman RR (1995) Seizure outcome after lesionectomy for cavernous malformations. J Neurosurg 83:237–242PubMedCrossRefGoogle Scholar
  21. Dasgupta R, Fishman SJ (2014) ISSVA classification. Semin Pediatr Surg 23:158–161PubMedCrossRefGoogle Scholar
  22. Di Giannatale A, Morana G, Rossi A, Cama A, Bertoluzzo L, Barra S, Nozza P, Milanaccio C, Consales A, Garrè ML (2014) Natural history of cavernous malformations in children with brain tumors treated with radiotherapy and chemotherapy. J Neuro-Oncol 117:311–320CrossRefGoogle Scholar
  23. Di Rocco C, Iannelli A, Tamburrini G (1996) Cavernomas of the central nervous system in children. A report of 22 cases. Acta Neurochir 138:1267–1274PubMedCrossRefGoogle Scholar
  24. Di Rocco C, Iannelli A, Tamburrini G (1997) Surgical management of paediatric cerebral cavernomas. J Neurosurg Sci 41:343–347PubMedGoogle Scholar
  25. Draheim KM, Fisher OS, Boggon TJ, Calderwood DA (2014) Cerebral cavernous malformation proteins at a glance. J Cell Sci 127:701–707PubMedPubMedCentralCrossRefGoogle Scholar
  26. Ene C, Kaul A, Kim L (2017) Natural history of cerebral cavernous malformations. Handb Clin Neurol 143:227–232PubMedCrossRefGoogle Scholar
  27. Englot DJ, Han SJ, Lawton MT, Chang EF (2011) Predictors of seizure freedom in the surgical treatment of supratentorial cavernous malformations. J Neurosurg 115:1169–1174PubMedCrossRefGoogle Scholar
  28. Ferroli P, Casazza M, Marras C, Mendola C, Franzini A, Broggi G (2006) Cerebral cavernomas and seizures: a retrospective study on 163 patients who underwent pure lesionectomy. Neurol Sci 26:390–394PubMedCrossRefGoogle Scholar
  29. Fischer A, Zalvide J, Faurobert E, Albiges-Rizo C, Tournier-Lasserve E (2013) Cerebral cavernous malformations: from CCM genes to endothelial cell homeostasis. Trends Mol Med 19:302–308PubMedCrossRefGoogle Scholar
  30. Flemming KD, Link MJ, Christianson TJ, Brown RD Jr (2013) Use of antithrombotic agents in patients with intracerebral cavernous malformations. J Neurosurg 118:43–46PubMedCrossRefGoogle Scholar
  31. Goitre L, De Luca E, Braggion S, Trapani E, Guglielmotto M, Biasi F, Forni M, Moglia A, Trabalzini L, Retta SF (2014) KRIT1 loss of function causes a ROS-dependent upregulation of c-Jun. Free Radic Biol Med 68:134–147PubMedPubMedCentralCrossRefGoogle Scholar
  32. Golden MJ, Morrison LA, Kim H, Hart BL (2015a) Increased number of white matter lesions in patients with familial cerebral cavernous malformations. AJNR 36:899–903PubMedCrossRefPubMedCentralGoogle Scholar
  33. Golden M, Saeidi S, Liem B, Marchand E, Morrison L, Hart B (2015b) Sensitivity of patients with familial cerebral cavernous malformations to therapeutic radiation. J Med Imaging Radiat Oncol 59:134–136PubMedPubMedCentralCrossRefGoogle Scholar
  34. Gross BA, Du R, Orbach DB, Scott RM, Smith ER (2015) The natural history of cerebral cavernous malformations in children. J Neurosur Pediatr 16:1–6Google Scholar
  35. Hammen T, Romstöck J, Dörfler A, Kerling F, Buchfelder M, Stefan H (2007) Prediction of postoperative outcome with special respect to removal of hemosiderin fringe: a study in patients with cavernous haemangiomas associated with symptomatic epilepsy. Seizure 16:248–253PubMedCrossRefPubMedCentralGoogle Scholar
  36. Heckl S, Aschoff A, Kunze S (2002) Radiation-induced cavernous hemangiomas of the brain: a late effect predominantly in children. Cancer 94:3285–3291PubMedCrossRefPubMedCentralGoogle Scholar
  37. Jakimovski D, Schneider H, Frei K, Kennes LN, Bertalanffy H (2014) Bleeding propensity of cavernous malformations: impact of tight junction alterations on the occurrence of overt hematoma. J Neurosurg 121:613–620PubMedCrossRefPubMedCentralGoogle Scholar
  38. Josephson C, Leach J, Duncan R, Roberts R, Counsell C, Salman R (2011) Seizure risk from cavernous or arteriovenous malformations prospective population-based study. Neurology 76:1548–1554PubMedPubMedCentralCrossRefGoogle Scholar
  39. Kar S, Samii A, Bertalanffy H (2015) PTEN/PI3K/Akt/VEGF signaling and the cross talk to KRIT1, CCM2, and PDCD10 proteins in cerebral cavernous malformations. Neurosurg Rev 38:229–236PubMedCrossRefPubMedCentralGoogle Scholar
  40. Kar S, Bali KK, Baisantry A, Geffers R, Samii A, Bertalanffy H (2017) Genome-wide sequencing reveals MicroRNAs downregulated in cerebral cavernous malformations. J Mol Neurosci 61:178–188PubMedCrossRefGoogle Scholar
  41. Kar S, Bali KK, Baisantry A, Geffers R, Hartmann C, Samii A, Bertalanffy H (2018) Genome-wide sequencing reveals small nucleolar RNAs downregulated in cerebral cavernous malformations. Cell Mol Neurobiol. Jul 10 (epub ahead of print).  https://doi.org/10.1007/s10571-018-0602-9CrossRefGoogle Scholar
  42. Kivelev J, Niemelä M, Blomstedt G, Roivainen R, Lehecka M, Hernesniemi J (2011) Microsurgical treatment of temporal lobe cavernomas. Acta Neurochir 153:261–270PubMedCrossRefGoogle Scholar
  43. Kleinschmidt-DeMasters BK, Lillehei KO (2016) Radiation-induced cerebral vascular “malformations” at biopsy. Neuropathol Exp Neurol 75:1081–1092CrossRefGoogle Scholar
  44. Knerlich-Lukoschus F, Steinbok P, Dunham C, Cochrane DD (2015) Cerebellar cavernous malformation in pediatric patients: defining clinical, neuroimaging, and therapeutic characteristics. J Neurosurg Pediatr 16:256–266PubMedCrossRefGoogle Scholar
  45. Kondziolka D, Lunsford LD, Kestle JR (1995) The natural history of cerebral cavernous malformations. J Neurosurg 83:820–824PubMedCrossRefGoogle Scholar
  46. Labauge P, Denier C, Bergametti F, Tournier-Lasserve E (2007) Genetics of cavernous angiomas. Lancet Neurol 6:237–244PubMedCrossRefGoogle Scholar
  47. Leaute-Labreze C, Dumas de la Roque E, Hubiche T, Boralevi F, Thambo JB, Taïeb A (2008) Propranolol for severe hemangiomas of infancy. N Engl J Med 358:2649–2651PubMedCrossRefGoogle Scholar
  48. Lisowska J, Rodel CJ, Manet S, Miroshnikova YA, Boyault C, Planus E, De Mets R, Lee HH, Destaing O, Mertani H, Boulday G, Tournier-Lasserve E, Balland M, Abdelilah-Seyfried S, Albiges-Rizo C, Faurobert E (2018) The CCM1-CCM2 complex controls complementary functions of ROCK1 and ROCK2 that are required for endothelial integrity. J Cell Sci 131(15):jcs216093PubMedCrossRefGoogle Scholar
  49. Liu HB, Wang Y, Yang S, Gong FL, Xu YY, Wang W (2016) Gamma knife radiosurgery for brainstem cavernous malformations. Clin Neurol Neurosurg 151:55–60PubMedCrossRefGoogle Scholar
  50. Lopez-Ramirez MA, Fonseca G, Zeineddine HA, Girard R, Moore T, Pham A, Cao Y, Shenkar R, de Kreuk BJ, Lagarrigue F, Lawler J, Glass CK, Awad IA, Ginsberg MH (2017) Thrombospondin1 (TSP1) replacement prevents cerebral cavernous malformations. J Exp Med 214:3331–3346PubMedPubMedCentralCrossRefGoogle Scholar
  51. Marchi S, Corricelli M, Trapani E, Bravi L, Pittaro A, Delle Monache S, Ferroni L, Patergnani S, Missiroli S, Goitre L, Trabalzini L, Rimessi A, Giorgi C, Zavan B, Cassoni P, Dejana E, Retta SF, Pinton P (2015) Defective autophagy is a key feature of cerebral cavernous malformations. EMBO Mol Med 7:1403–1417PubMedPubMedCentralCrossRefGoogle Scholar
  52. Massimi L, Battaglia D, Bianchi F, Peraio S, Peppucci E, Di Rocco C (2018) Postoperative epileptic seizures in children: is the brain incision a risk factor? Neurosurgery 82:465–472PubMedCrossRefGoogle Scholar
  53. Meng G, Bai C, Yu T, Wu Z, Liu X, Zhang J, Zhao J (2014) The association between cerebral developmental venous anomaly and concomitant cavernous malformation: an observational study using magnetic resonance imaging. BMC Neurol 14:50PubMedPubMedCentralCrossRefGoogle Scholar
  54. Mikati AG, Tan H, Shenkar R, Li L, Zhang L, Guo X, Larsson HB, Shi C, Liu T, Wang Y, Shah A, Edelman RR, Christoforidis G, Awad I (2014) Dynamic permeability and quantitative susceptibility: related imaging biomarkers in cerebral cavernous malformations. Stroke 45:598–601PubMedCrossRefGoogle Scholar
  55. Miquel J, Bruneau B, Dupuy A (2014) Successful treatment of multifocal intracerebral and spinal hemangiomas with propranolol. J Am Acad Dermatol 70:e83–e84PubMedCrossRefGoogle Scholar
  56. Mokin M, Agazzi S, Dawson L, Primiani CT (2017) Neuroimaging of cavernous malformations. Curr Pain Headache Rep 21:47PubMedCrossRefGoogle Scholar
  57. Moore SA, Brown RD Jr, Christianson TJ, Flemming KD (2014) Long-term natural history of incidentally discovered cavernous malformations in a single-center cohort. J Neurosurg 120:1188–1192PubMedCrossRefGoogle Scholar
  58. Moran NF, Fish DR, Kitchen N, Shorvon S, Kendall BE, Stevens JM (1999) Supratentorial cavernous haemangiomas and epilepsy: a review of the literature and case series. J Neurol Neurosurg Psychiatry 66:561–568PubMedPubMedCentralCrossRefGoogle Scholar
  59. Moschovi M, Alexiou GA, Tourkantoni N, Prodromou N (2010) Propranolol treatment for a giant infantile brain cavernoma. J Child Neurol 25:653–655PubMedCrossRefGoogle Scholar
  60. Mottolese C, Hermier M, Stan H, Jouvet A, Saint-Pierre G, Froment JC, Bret P, Lapras C (2001) Central nervous system cavernomas in the pediatric age group. Neurosurg Rev 24:55–71PubMedCrossRefGoogle Scholar
  61. Mouchtouris N, Chalouhi N, Chitale A, Starke RM, Tjoumakaris SI, Rosenwasser RH, Jabbour PM (2015) Management of cerebral cavernous malformations: from diagnosis to treatment. Sci World J 2015:808314CrossRefGoogle Scholar
  62. Nagy G, Kemeny AA (2013) Stereotactic radiosurgery of intracranial cavernous malformations. Neurosurg Clin N Am 24:575–589PubMedCrossRefGoogle Scholar
  63. Nikoubashman O, Wiesmann M, Tournier-Lasserve E, Mankad K, Bourgeois M, Brunelle F, Sainte-Rose C, Wiesmann M, Zerah M, Di Rocco F (2013) Natural history of cerebral dot-like cavernomas. Clin Radiol 68:e453–e459PubMedCrossRefGoogle Scholar
  64. Nikoubashman O, Di Rocco F, Davagnanam I, Mankad K, Zerah M, Wiesmann M (2015) Prospective hemorrhage rates of cerebral cavernous malformations in children and adolescents based on MRI appearance. Am J Neuroradiol 36: 2177–2783PubMedCrossRefGoogle Scholar
  65. Osborn AG (2016) Cavernous malformation. In: Osborn AG, Salzman KL, Jhaveri MD (eds) Diagnostic imaging: brain, 3rd edn. Elsevier, Philadelphia, pp 420–423Google Scholar
  66. Otten P, Pizzolato GP, Rilliet B, Berney J (1989) 131 cases of cavernous angioma (cavernomas) of the CNS, discovered by retrospective analysis of 24,535 autopsies. Neurochirurgie 35:82–83. (article in French)PubMedGoogle Scholar
  67. Patel PA, Amin-Hanjani S, Ogilvy SC (2012) Surgical management of cavernous malformations of the nervous system. In: Quiñones-Hinoiosa A (ed) Schmidek and sweet operative neurosurgical techniques, 6th edn. Elsevier, Philadelphia, pp 977–993CrossRefGoogle Scholar
  68. Phuong PC, Luan ND, Trang VTH, Schild SE, Rades D, Khoa MT (2017) Radiosurgery with a rotating gamma system: a very effective treatment for symptomatic cerebral cavernomas. Anticancer Res 37:3729–3733PubMedGoogle Scholar
  69. Qiao N, Ma Z, Song J, Wang Y, Shou X, Zhang X, Shen M, Qiu H, Ye Z, He W, Li S, Fu C, Zhao Y (2015) A systematic review and meta-analysis of surgeries performed for treating deep-seated cerebral cavernous malformations. Br J Neurosurg 29:493–499PubMedCrossRefGoogle Scholar
  70. Recalde RJ, Figueiredo EG, de Oliveira E (2008) Microsurgical anatomy of the safe entry zones on the anterolateral brainstem related to surgical approaches to cavernous malformations. Neurosurgery 62:9–15PubMedGoogle Scholar
  71. Reinhard M, Schuchardt F, Meckel S, Heinz J, Felbor U, Sure U, Geisen U (2016) Propranolol stops progressive multiple cerebral cavernoma in an adult patient. J Neurol Sci 367:15–17PubMedCrossRefGoogle Scholar
  72. Revencu N, Vikkula M (2006) Cerebral cavernous malformation: new molecular and clinical insights. J Med Genet 43:716–721PubMedPubMedCentralCrossRefGoogle Scholar
  73. Riant F, Bergametti F, Ayrignac X, Boulday G, Tournier-Lasserve E (2010) Recent insights into cerebral cavernous malformations: the molecular genetics of CCM. FEBS J 277:1070–1075PubMedCrossRefGoogle Scholar
  74. Robinson JR, Awad IA, Little JR (1991) Natural history of the cavernous angioma. J Neurosurg 75:709–714PubMedCrossRefGoogle Scholar
  75. Rosenow F, Alonso-Vanegas MA, Baumgartner C, Blumcke I, Carreno M, Gizewski ER, Hamer HM, Knake S, Kahane P, Luders HO, Mathern GW, Menzler K, Miller J, Otsuki T, Ozkara C, Pitkanen A, Roper SN, Sakamoto AC, Sure U, Walker MC, Steinhoff BJ (2013) Cavernoma-related epilepsy: review and recommendations for management – report of the surgical task force of the ILAE commission on therapeutic strategies. Epilepsia 54:2025–2035PubMedCrossRefGoogle Scholar
  76. Russell D, Rubinstein L (1989) Pathology of tumours of the nervous system, 5th edn. Edward Arnold, London, pp 730–746Google Scholar
  77. Samii M, Eghbal R, Carvalho GA, Matthies C (2001) Surgical management of brainstem cavernomas. J Neurosurg 95:825–832PubMedCrossRefGoogle Scholar
  78. Schneider BF, Eberhard DA, Steiner LE (1997) Histopathology of arteriovenous malformations after gamma knife radiosurgery. J Neurosurg 87:352–357PubMedCrossRefPubMedCentralGoogle Scholar
  79. Scott RM, Barnes P, Kupsky W, Adelman LS (1992) Cavernous angiomas of the central nervous system in children. J Neurosurg 76:38–46PubMedCrossRefPubMedCentralGoogle Scholar
  80. Sharma V, Babu PP, Singh A, Singh S, Singh R (2007) Iron induced experimental cortical seizures: electroencephalographic mapping of seizure spread in the subcortical brain areas. Seizures 16:680–690CrossRefGoogle Scholar
  81. Sommer B, Kasper BS, Coras R, Blumcke I, Hamer HM, Buchfelder M, Roessler K (2013) Surgical management of epilepsy due to cerebral cavernomas using neuronavigation and intraoperative MR imaging. Neurol Res 35:1076–1083PubMedPubMedCentralCrossRefGoogle Scholar
  82. Sommers Smith SK, Smith DM (2002) Beta blockade induces apoptosis in cultured capillary endothelial cells. In Vitro Cell Dev Biol Anim 38:298–304PubMedCrossRefGoogle Scholar
  83. Stavrou I, Baumgartner C, Frischer JM, Trattnig S, Knosp E (2008) Long-term seizure control after resection of supratentorial cavernomas: a retrospective single-center study in 53 patients. Neurosurgery 63:888–896PubMedCrossRefGoogle Scholar
  84. Tang AT, Choi JP, Kotzin JJ, Yang Y, Hong CC, Hobson N, Girard R, Zeineddine HA, Lightle R, Moore T, Cao Y, Shenkar R, Chen M, Mericko P, Yang J, Li L, Tanes C, Kobuley D, Võsa U, Whitehead KJ, Li DY, Franke L, Hart B, Schwaninger M, Henao-Mejia J, Morrison L, Kim H, Awad IA, Zheng X, Kahn ML (2017) Endothelial TLR4 and the microbiome drive cerebral cavernous malformations. Nature 545:305–310PubMedPubMedCentralCrossRefGoogle Scholar
  85. Tirakotai W, Sure U, Benes L, Krischek B, Bien S, Bertalanffy H (2003) Image-guided transsylvian, transinsular approach for insular cavernous angiomas. Neurosurgery 53:1299–1305PubMedCrossRefGoogle Scholar
  86. Tirakotai W, Fremann S, Soerensen N, Roggendorf W, Siegel AM, Mennel HD, Zhu Y, Bertalanffy H, Sure U (2006) Biological activity of paediatric cerebral cavernomas: an immunohistochemical study of 28 patients. Childs Nerv Syst 22:685–691PubMedCrossRefGoogle Scholar
  87. Ulrich NH, Kockro RA, Bellut D, Amaxopoulou C, Bozinov O, Burkhardt JK, Sarnthein J, Kollias SS, Bertalanffy H (2014) Brainstem cavernoma surgery with the support of pre- and postoperative diffusion tensor imaging: initial experiences and clinical course of 23 patients. Neurosurg Rev 37:481–491PubMedCrossRefGoogle Scholar
  88. Van Gompel JJ, Rubio J, Cascino GD, Worrell GA, Meyer JB (2009) Electrocorticography guided resection of temporal cavernoma: is electrocorticography warranted and does it alter the surgical approach? J Neurosurg 110:1179–1185PubMedPubMedCentralCrossRefGoogle Scholar
  89. Villanueva P, Louis RG, Cutler AR, Wei H, Sale D, Duong HT, Barkhoudarian G, Kelly DF (2015) Endoscopic and gravity-assisted resection of medial temporo-occipital lesions through a supracerebellar transtentorial approach: technical notes with case illustrations. Oper Neurosurg (Hagerstown) 11:475–483CrossRefGoogle Scholar
  90. Vinchon M, Leblond P, Caron S, Delestret I, Baroncini M, Coche B (2011) Radiation-induced tumors in children irradiated for brain tumor: a longitudinal study. Childs Nerv Syst 27:445–453PubMedCrossRefGoogle Scholar
  91. Wang CC, Liu A, Zhang JT, Sun B, Zhao YL (2003) Surgical management of brain-stem cavernous malformations: report of 137cases. Surg Neurol 59:444–454PubMedCrossRefGoogle Scholar
  92. Wang X, Tao Z, You C, Yi Liu QL (2013) Extended resection of hemosiderin fringe is better for seizure outcome: a study in patients with cavernous malformation associated with refractory epilepsy. Neurol India 61:288–292PubMedCrossRefGoogle Scholar
  93. Wassef M, Blei F, Adams D, Alomari A, Baselga E, Berenstein A, Burrows P, Frieden IJ, Garzon MC, Lopez-Gutierrez JC, Lord DJE, Mitchel S, Powell J, Prendiville J, Vikkula M (2015) Vascular anomalies classification: recommendations from the International Society for the Study of Vascular Anomalies. Pediatrics 136:e203PubMedCrossRefGoogle Scholar
  94. Xia C, Zhang R, Mao Y, Zhou L (2009) Pediatric cavernous malformation in the central nervous system: report of 66 cases. Pediatr Neurosurg 45:105–113PubMedCrossRefGoogle Scholar
  95. Young A, Poretti A, Bosemani T, Goel R, Huisman TAGM (2017) Sensitivity of susceptibility-weighted imaging in detecting developmental venous anomalies and associated cavernomas and microhemorrhages in children. Neuroradiology 59:797–802PubMedCrossRefGoogle Scholar
  96. Zabramski JM, Wascher TM, Spetzler RF, Johnson B, Golfinos J, Drayer BP, Brown B, Rigamonti D, Brown G (1994) The natural history of familial cavernous malformations: results of an ongoing study. J Neurosurg 80:422–432PubMedCrossRefGoogle Scholar
  97. Zabramski JM, Kalani MY, Filippidis AS, Spetzler RF (2016) Propranolol treatment of cavernous malformations with symptomatic hemorrhage. World Neurosurg 88:631–639PubMedCrossRefGoogle Scholar
  98. Zhou HJ, Qin L, Zhang H, Tang W, Ji W, He Y, Liang X, Wang Z, Yuan Q, Vortmeyer A, Toomre D, Fuh G, Yan M, Kluger MS, Wu D, Min W (2016) Augmented endothelial exocytosis of angiopoietin-2 resulting from CCM3-deficiency contributes to the progression of cerebral cavernous malformation. Nat Med 22:1033–1042CrossRefGoogle Scholar
  99. Zhu WZ, Qi JP, Zhan CJ, Shu HG, Zhang L, Wang CY, Xia LM, Hu JW, Feng DY (2008) Magnetic resonance susceptibility weighted imaging in detecting intracranial calcification and hemorrhage. Chin Med J 121:2021–2025PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Luca Massimi
    • 1
    Email author
  • Souvik Kar
    • 2
  • Mario Giordano
    • 2
  • Helmut Bertalanffy
    • 2
  1. 1.Pediatric NeurosurgeryFondazione Policlinico A. Gemelli IRCCSRomeItaly
  2. 2.International Neuroscience Institute (INI)HannoverGermany

Section editors and affiliations

  • Concezio Di Rocco
    • 1
  1. 1.Department of NeurosurgeryInternational Neuroscience InstituteHannoverGermany

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