Advertisement

Spinal Cord Tumors in Neurofacomatosis

  • Frederick A. Boop
  • Jimmy Ming-Jung Chuang
  • Chenran Zhang
Chapter
  • 483 Downloads

Abstract

Neurofacomatosis (phakomatoses) are a group of neuro-oculocutaneous disorders characterized by involvement of structures that arise from the embryonic ectoderm—thus, the central nervous system (CNS), skin, and eyes. The phakomatoses concept was formulated in 1923 by ophthalmologist Van Der Hoeve to describe three disorders (neurofibromatosis, tuberous sclerosis, and von Hippel-Lindau syndrome) according to their ophthalmologic manifestations (Greek phakos means birthmark). However, it has been subsequently noted that mesodermal and endodermal tissues are also involved. A number of genetic and acquired diseases come in this category and may affect one or more organ systems. They tend to form tumors in various organs, particular the nervous system. Now, neurofacomatosis are also termed as “neuroectodermatoses” or “neurocutaneous syndrome.” Intramedullary spinal cord tumors are rare. They account for only 4–6% of all CNS tumors. In this chapter, we survey the neurocutaneous tumor syndrome and intramedullary spinal cord tumor associated with the three major neurofacomatosis: Neurofibromatosis type I (NF1), Neurofibromatosis type 2 (NF2), and von Hippel-Lindau syndrome (VHL).

Keywords

Neurofacomatosis Phakomatoses Neurofibromatosis Tuberous sclerosis von Hippel-Lindau syndrome 

References

  1. 1.
    Van Der Hoeve J. Les phacomatoses de Bourneville, de Recklinghausen at de von Hippel-Lindau. J Beige Neurol Psychiatr. 1933;33:752.Google Scholar
  2. 2.
    Van Der Hoeve J. Eye diseases in tuberous sclerosis of the brain and in Recklinghausen disease. Trans Ophthalmol Soc UK. 1923;43:534.Google Scholar
  3. 3.
    Russell DS, Rubinstein LJ. Pathology of Tumors of the Nervous System. 5th ed. London: Edward Arnold; 1989.Google Scholar
  4. 4.
    Von Recklinghausen F. Ueber die multiplen Fibrome der Haut und ihre Beziehung zu den multiplen Neuromen. Berlin: Verlag von August Hirschwald; 1882.Google Scholar
  5. 5.
    Korf BR. Clinical features and pathobiology of neurofibromatosis 1. J Child Neurol. 2002;17(8):573–7.; discussion 602-574, 646-551.  https://doi.org/10.1177/088307380201700806.CrossRefPubMedGoogle Scholar
  6. 6.
    Lammert M, Friedman JM, Kluwe L, Mautner VF. Prevalence of neurofibromatosis 1 in German children at elementary school enrollment. Arch Dermatol. 2005;141(1):71–4.  https://doi.org/10.1001/archderm.141.1.71.CrossRefGoogle Scholar
  7. 7.
    North K. Neurofibromatosis type 1: review of the first 200 patients in an Australian clinic. J Child Neurol. 1993;8(4):395–402.  https://doi.org/10.1177/088307389300800421.CrossRefPubMedGoogle Scholar
  8. 8.
    DeBella K, Szudek J, Friedman JM. Use of the national institutes of health criteria for diagnosis of neurofibromatosis 1 in children. Pediatrics. 2000;105(3 Pt 1):608–14.Google Scholar
  9. 9.
    Poyhonen M, Niemela S, Herva R. Risk of malignancy and death in neurofibromatosis. Arch Pathol Lab Med. 1997;121(2):139–43.PubMedGoogle Scholar
  10. 10.
    Farrell CJ, Plotkin SR. Genetic causes of brain tumors: neurofibromatosis, tuberous sclerosis, von Hippel-Lindau, and other syndromes. Neurol Clin. 2007;25(4):925–46., viii.  https://doi.org/10.1016/j.ncl.2007.07.008.CrossRefPubMedGoogle Scholar
  11. 11.
    Pros E, Gomez C, Martin T, Fabregas P, Serra E, Lazaro C. Nature and mRNA effect of 282 different NF1 point mutations: focus on splicing alterations. Hum Mutat. 2008;29(9):E173–93.  https://doi.org/10.1002/humu.20826.CrossRefGoogle Scholar
  12. 12.
    Cawthon RM, Weiss R, Xu GF, Viskochil D, Culver M, Stevens J, Robertson M, Dunn D, Gesteland R, O'Connell P, et al. A major segment of the neurofibromatosis type 1 gene: cDNA sequence, genomic structure, and point mutations. Cell. 1990;62(1):193–201.Google Scholar
  13. 13.
    Li Y, O'Connell P, Breidenbach HH, Cawthon R, Stevens J, Xu G, Neil S, Robertson M, White R, Viskochil D. Genomic organization of the neurofibromatosis 1 gene (NF1). Genomics. 1995;25(1):9–18.Google Scholar
  14. 14.
    Daston MM, Scrable H, Nordlund M, Sturbaum AK, Nissen LM, Ratner N. The protein product of the neurofibromatosis type 1 gene is expressed at highest abundance in neurons, Schwann cells, and oligodendrocytes. Neuron. 1992;8(3):415–28.Google Scholar
  15. 15.
    Zhu Y, Ghosh P, Charnay P, Burns DK, Parada LF. Neurofibromas in NF1: Schwann cell origin and role of tumor environment. Science. 2002;296(5569):920–2.  https://doi.org/10.1126/science.1068452.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Gutmann DH, Donahoe J, Brown T, James CD, Perry A. Loss of neurofibromatosis 1 (NF1) gene expression in NF1-associated pilocytic astrocytomas. Neuropathol Appl Neurobiol. 2000;26(4):361–7.PubMedGoogle Scholar
  17. 17.
    Hutt-Cabezas M, Karajannis MA, Zagzag D, Shah S, Horkayne-Szakaly I, Rushing EJ, Cameron JD, Jain D, Eberhart CG, Raabe EH, Rodriguez FJ. Activation of mTORC1/mTORC2 signaling in pediatric low-grade glioma and pilocytic astrocytoma reveals mTOR as a therapeutic target. Neuro-Oncology. 2013;15(12):1604–14.  https://doi.org/10.1093/neuonc/not132.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Daras M, Kaley TJ. Benign brain tumors and tumors associated with phakomatoses. Continuum (Minneap Minn). 2015; 21(2 Neuro-oncology):397–414.  https://doi.org/10.1212/01.CON.0000464177.73440.44.
  19. 19.
    American Academy of Pediatrics Committee on Genetics. Health supervision for children with neurofibromatosis. Pediatrics. 1995;96(2 Pt 1):368–72.Google Scholar
  20. 20.
    Yohay K. Neurofibromatosis type 1 and associated malignancies. Curr Neurol Neurosci Rep. 2009;9(3):247–53.PubMedGoogle Scholar
  21. 21.
    Walker L, Thompson D, Easton D, Ponder B, Ponder M, Frayling I, Baralle D. A prospective study of neurofibromatosis type 1 cancer incidence in the UK. Br J Cancer. 2006;95(2):233–8.  https://doi.org/10.1038/sj.bjc.6603227.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Nguyen R, Dombi E, Akshintala S, Baldwin A, Widemann BC. Characterization of spinal findings in children and adults with neurofibromatosis type 1 enrolled in a natural history study using magnetic resonance imaging. J Neuro-Oncol. 2015;121(1):209–15.  https://doi.org/10.1007/s11060-014-1629-5.CrossRefGoogle Scholar
  23. 23.
    Abul-Kasim K, Thurnher MM, McKeever P, Sundgren PC. Intradural spinal tumors: current classification and MRI features. Neuroradiology. 2008;50(4):301–14.  https://doi.org/10.1007/s00234-007-0345-7.CrossRefPubMedGoogle Scholar
  24. 24.
    Carey JC, Viskochil DH. Neurofibromatosis type 1: A model condition for the study of the molecular basis of variable expressivity in human disorders. Am J Med Genet. 1999;89(1):7–13.PubMedGoogle Scholar
  25. 25.
    Riccardi VM. Neurofibromatosis, Phenotype, Natural History, and Pathogenesis. 2nd ed. Baltimore: Johns Hopkins University Press; 1992.Google Scholar
  26. 26.
    Nguyen R, Dombi E, Widemann BC, Solomon J, Fuensterer C, Kluwe L, Friedman JM, Mautner VF. Growth dynamics of plexiform neurofibromas: a retrospective cohort study of 201 patients with neurofibromatosis 1. Orphanet J Rare Dis. 2012;7:75.  https://doi.org/10.1186/1750-1172-7-75.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Thakkar SD, Feigen U, Mautner VF. Spinal tumours in neurofibromatosis type 1: an MRI study of frequency, multiplicity and variety. Neuroradiology. 1999;41(9):625–9.Google Scholar
  28. 28.
    Jinnai T, Koyama T. Clinical characteristics of spinal nerve sheath tumors: analysis of 149 cases. Neurosurgery. 2005;56(3):510–5. discussion 510-515PubMedGoogle Scholar
  29. 29.
    Guillamo JS, Creange A, Kalifa C, Grill J, Rodriguez D, Doz F, Barbarot S, Zerah M, Sanson M, Bastuji-Garin S, Wolkenstein P, Reseau NFF. Prognostic factors of CNS tumours in Neurofibromatosis 1 (NF1): a retrospective study of 104 patients. Brain. 2003;126(Pt 1):152–60.Google Scholar
  30. 30.
    Rosenfeld A, Listernick R, Charrow J, Goldman S. Neurofibromatosis type 1 and high-grade tumors of the central nervous system. Childs Nerv Syst. 2010;26(5):663–7.  https://doi.org/10.1007/s00381-009-1024-2.CrossRefPubMedGoogle Scholar
  31. 31.
    Rasmussen SA, Yang Q, Friedman JM. Mortality in neurofibromatosis 1: an analysis using U.S. death certificates. Am J Hum Genet. 2001;68(5):1110–8.  https://doi.org/10.1086/320121.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Lee M, Rezai AR, Freed D, Epstein FJ. Intramedullary spinal cord tumors in neurofibromatosis. Neurosurgery. 1996;38(1):32–7.Google Scholar
  33. 33.
    Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW. The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol. 2016;131(6):803–20.  https://doi.org/10.1007/s00401-016-1545-1.CrossRefPubMedGoogle Scholar
  34. 34.
    Gutmann DH, Rasmussen SA, Wolkenstein P, MacCollin MM, Guha A, Inskip PD, North KN, Poyhonen M, Birch PH, Friedman JM. Gliomas presenting after age 10 in individuals with neurofibromatosis type 1 (NF1). Neurology. 2002;59(5):759–61.Google Scholar
  35. 35.
    Rodriguez FJ, Perry A, Gutmann DH, O'Neill BP, Leonard J, Bryant S, Giannini C. Gliomas in neurofibromatosis type 1: a clinicopathologic study of 100 patients. J Neuropathol Exp Neurol. 2008;67(3):240–9.  https://doi.org/10.1097/NEN.0b013e318165eb75.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Mendiratta-Lala M, Kader Ellika S, Gutierrez JA, Patel SC, Jain R. Spinal cord pilomyxoid astrocytoma: an unusual tumor. J Neuroimaging. 2007;17(4):371–4.  https://doi.org/10.1111/j.1552-6569.2006.00101.x.CrossRefPubMedGoogle Scholar
  37. 37.
    Dunn-Pirio AM, Howell E, McLendon RE, Peters KB. Single-Agent Carboplatin for a Rare Case of Pilomyxoid Astrocytoma of the Spinal Cord in an Adult with Neurofibromatosis Type 1. Case Rep Oncol. 2016;9(3):568–73.  https://doi.org/10.1159/000449406.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Cheng H, Shan M, Feng C, Wang X. Spinal cord ependymoma associated with neurofibromatosis 1 : case report and review of the literature. J Korean Neurosurg Soc. 2014;55(1):43–7.  https://doi.org/10.3340/jkns.2014.55.1.43.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Riffaud L, Vinchon M, Ragragui O, Delestret I, Ruchoux MM, Dhellemmes P. Hemispheric cerebral gliomas in children with NF1: arguments for a long-term follow-up. Childs Nerv Syst. 2002;18(1–2):43–7.  https://doi.org/10.1007/s00381-001-0534-3.CrossRefPubMedGoogle Scholar
  40. 40.
    Mittal A, Meena R, Samar N, Kumar S, Khandelwal A. A Case of Neurofibromatosis Type 1 Associated with Cervical Cord Ependymoma. Int J Curr Res Rev. 2017;9(23):22–4.Google Scholar
  41. 41.
    Evans DG, Moran A, King A, Saeed S, Gurusinghe N, Ramsden R. Incidence of vestibular schwannoma and neurofibromatosis 2 in the North West of England over a 10-year period: higher incidence than previously thought. Otol Neurotol. 2005;26(1):93–7.PubMedGoogle Scholar
  42. 42.
    Evans DG. Neurofibromatosis type 2 (NF2): a clinical and molecular review. Orphanet J Rare Dis. 2009;4:16.  https://doi.org/10.1186/1750-1172-4-16.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Evans DG, Birch JM, Ramsden RT. Paediatric presentation of type 2 neurofibromatosis. Arch Dis Child. 1999;81(6):496–9.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Rouleau GA, Merel P, Lutchman M, Sanson M, Zucman J, Marineau C, Hoang-Xuan K, Demczuk S, Desmaze C, Plougastel B, et al. Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature. 1993;363(6429):515–21.  https://doi.org/10.1038/363515a0.CrossRefPubMedGoogle Scholar
  45. 45.
    Xiao GH, Chernoff J, Testa JR. NF2: the wizardry of merlin. Genes Chromosomes Cancer. 2003;38(4):389–99.  https://doi.org/10.1002/gcc.10282.CrossRefPubMedGoogle Scholar
  46. 46.
    Cooper J, Giancotti FG. Molecular insights into NF2/Merlin tumor suppressor function. FEBS Lett. 2014;588(16):2743–52.  https://doi.org/10.1016/j.febslet.2014.04.001.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Parry DM, MacCollin MM, Kaiser-Kupfer MI, Pulaski K, Nicholson HS, Bolesta M, Eldridge R, Gusella JF. Germ-line mutations in the neurofibromatosis 2 gene: correlations with disease severity and retinal abnormalities. Am J Hum Genet. 1996;59(3):529–39.PubMedPubMedCentralGoogle Scholar
  48. 48.
    Baser ME, Friedman JM, Wallace AJ, Ramsden RT, Joe H, Evans DG. Evaluation of clinical diagnostic criteria for neurofibromatosis 2. Neurology. 2002;59(11):1759–65.PubMedGoogle Scholar
  49. 49.
    Evans DG, Raymond FL, Barwell JG, Halliday D. Genetic testing and screening of individuals at risk of NF2. Clin Genet. 2012;82(5):416–24.  https://doi.org/10.1111/j.1399-0004.2011.01816.x.CrossRefPubMedGoogle Scholar
  50. 50.
    Campian J, Gutmann DH. CNS Tumors in Neurofibromatosis. J Clin Oncol. 2017;35(21):2378–85.  https://doi.org/10.1200/JCO.2016.71.7199.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Evans DG, Huson SM, Donnai D, Neary W, Blair V, Newton V, Harris R. A clinical study of type 2 neurofibromatosis. Q J Med. 1992;84(304):603–18.PubMedGoogle Scholar
  52. 52.
    Moffat DA, Quaranta N, Baguley DM, Hardy DG, Chang P. Management strategies in neurofibromatosis type 2. Eur Arch Otorhinolaryngol. 2003;260(1):12–8.  https://doi.org/10.1007/s00405-002-0503-9.CrossRefPubMedGoogle Scholar
  53. 53.
    Rowe JG, Radatz MW, Walton L, Soanes T, Rodgers J, Kemeny AA. Clinical experience with gamma knife stereotactic radiosurgery in the management of vestibular schwannomas secondary to type 2 neurofibromatosis. J Neurol Neurosurg Psychiatry. 2003;74(9):1288–93.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Ruggieri M, Iannetti P, Polizzi A, La Mantia I, Spalice A, Giliberto O, Platania N, Gabriele AL, Albanese V, Pavone L. Earliest clinical manifestations and natural history of neurofibromatosis type 2 (NF2) in childhood: a study of 24 patients. Neuropediatrics. 2005;36(1):21–34.  https://doi.org/10.1055/s-2005-837581.CrossRefGoogle Scholar
  55. 55.
    Malis LI. Neurofibromatosis type 2 and central neurofibromatosis. Neurosurg Focus. 1998;4(3):e1.PubMedGoogle Scholar
  56. 56.
    Nowak A, Dziedzic T, Czernicki T, Kunert P, Marchel A. Clinical course and management of intracranial meningiomas in neurofibromatosis type 2 patients. Neurol Neurochir Pol. 2015;49(6):367–72.  https://doi.org/10.1016/j.pjnns.2015.08.007.CrossRefPubMedGoogle Scholar
  57. 57.
    Wentworth S, Pinn M, Bourland JD, Deguzman AF, Ekstrand K, Ellis TL, Glazier SS, McMullen KP, Munley M, Stieber VW, Tatter SB, Shaw EG. Clinical experience with radiation therapy in the management of neurofibromatosis-associated central nervous system tumors. Int J Radiat Oncol Biol Phys. 2009;73(1):208–13.  https://doi.org/10.1016/j.ijrobp.2008.03.073.CrossRefPubMedGoogle Scholar
  58. 58.
    Perry A, Giannini C, Raghavan R, Scheithauer BW, Banerjee R, Margraf L, Bowers DC, Lytle RA, Newsham IF, Gutmann DH. Aggressive phenotypic and genotypic features in pediatric and NF2-associated meningiomas: a clinicopathologic study of 53 cases. J Neuropathol Exp Neurol. 2001;60(10):994–1003.PubMedGoogle Scholar
  59. 59.
    Halliday AL, Sobel RA, Martuza RL. Benign spinal nerve sheath tumors: their occurrence sporadically and in neurofibromatosis types 1 and 2. J Neurosurg. 1991;74(2):248–53.  https://doi.org/10.3171/jns.1991.74.2.0248.CrossRefPubMedGoogle Scholar
  60. 60.
    Klekamp J, Samii M. Surgery of spinal nerve sheath tumors with special reference to neurofibromatosis. Neurosurgery. 1998;42(2):279–89. discussion 289-290PubMedGoogle Scholar
  61. 61.
    Li P, Zhao F, Zhang J, Wang Z, Wang X, Wang B, Yang Z, Yang J, Gao Z, Liu P. Clinical features of spinal schwannomas in 65 patients with schwannomatosis compared with 831 with solitary schwannomas and 102 with neurofibromatosis Type 2: a retrospective study at a single institution. J Neurosurg Spine. 2016;24(1):145–54.  https://doi.org/10.3171/2015.3.SPINE141145.CrossRefPubMedGoogle Scholar
  62. 62.
    Mautner VF, Tatagiba M, Lindenau M, Funsterer C, Pulst SM, Baser ME, Kluwe L, Zanella FE. Spinal tumors in patients with neurofibromatosis type 2: MR imaging study of frequency, multiplicity, and variety. AJR Am J Roentgenol. 1995;165(4):951–5.  https://doi.org/10.2214/ajr.165.4.7676998.CrossRefPubMedGoogle Scholar
  63. 63.
    Aboukais R, Baroncini M, Zairi F, Bonne NX, Schapira S, Vincent C, Lejeune JP. Prognostic value and management of spinal tumors in neurofibromatosis type 2 patients. Acta Neurochir. 2013;155(5):771–7.  https://doi.org/10.1007/s00701-012-1590-z.CrossRefPubMedGoogle Scholar
  64. 64.
    Goutagny S, Kalamarides M. Meningiomas and neurofibromatosis. J Neuro-Oncol. 2010;99(3):341–7.  https://doi.org/10.1007/s11060-010-0339-x.CrossRefGoogle Scholar
  65. 65.
    Setzer M, Vatter H, Marquardt G, Seifert V, Vrionis FD. Management of spinal meningiomas: surgical results and a review of the literature. Neurosurg Focus. 2007;23(4):E14.  https://doi.org/10.3171/FOC-07/10/E14.CrossRefGoogle Scholar
  66. 66.
    Chang UK, Choe WJ, Chung SK, Chung CK, Kim HJ. Surgical outcome and prognostic factors of spinal intramedullary ependymomas in adults. J Neuro-Oncol. 2002;57(2):133–9.Google Scholar
  67. 67.
    Kalamarides M, Essayed W, Lejeune JP, Aboukais R, Sterkers O, Bernardeschi D, Peyre M, Lloyd SK, Freeman S, Hammerbeck-Ward C, Kellett M, Rutherford SA, Evans DG, Pathmanaban O, King AT. Spinal ependymomas in NF2: a surgical disease? J Neuro-Oncol. 2018;136(3):605–11.  https://doi.org/10.1007/s11060-017-2690-7.CrossRefGoogle Scholar
  68. 68.
    Hoshimaru M, Koyama T, Hashimoto N, Kikuchi H. Results of microsurgical treatment for intramedullary spinal cord ependymomas: analysis of 36 cases. Neurosurgery. 1999;44(2):264–9.PubMedGoogle Scholar
  69. 69.
    Plotkin SR, O'Donnell CC, Curry WT, Bove CM, MacCollin M, Nunes FP. Spinal ependymomas in neurofibromatosis Type 2: a retrospective analysis of 55 patients. J Neurosurg Spine. 2011;14(4):543–7.  https://doi.org/10.3171/2010.11.SPINE10350.CrossRefPubMedGoogle Scholar
  70. 70.
    Farschtschi S, Merker VL, Wolf D, Schuhmann M, Blakeley J, Plotkin SR, Hagel C, Mautner VF. Bevacizumab treatment for symptomatic spinal ependymomas in neurofibromatosis type 2. Acta Neurol Scand. 2016;133(6):475–80.  https://doi.org/10.1111/ane.12490.CrossRefPubMedGoogle Scholar
  71. 71.
    von Hippel E. Über eine sehr seltene Erkrankung der Netzhaut. Klin Beobachtungen Arch Ophthalmol. 1904;59(1):83–106.Google Scholar
  72. 72.
    Lindau A. Zur Frage der Angiomatosis Retinae und ihrer Hirnkomplikationen. Acta Ophthalmol. 1926;4(1–2):193–226.Google Scholar
  73. 73.
    Maher ER, Yates JR, Harries R, Benjamin C, Harris R, Moore AT, Ferguson-Smith MA. Clinical features and natural history of von Hippel-Lindau disease. Q J Med. 1990;77(283):1151–63.PubMedGoogle Scholar
  74. 74.
    Maher ER, Iselius L, Yates JR, Littler M, Benjamin C, Harris R, Sampson J, Williams A, Ferguson-Smith MA, Morton N. Von Hippel-Lindau disease: a genetic study. J Med Genet. 1991;28(7):443–7.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Kley N, Whaley J, Seizinger BR. Neurofibromatosis type 2 and von Hippel-Lindau disease: from gene cloning to function. Glia. 1995;15(3):297–307.  https://doi.org/10.1002/glia.440150310.CrossRefPubMedGoogle Scholar
  76. 76.
    Kim WY, Kaelin WG. Role of VHL gene mutation in human cancer. J Clin Oncol. 2004;22(24):4991–5004.  https://doi.org/10.1200/JCO.2004.05.061.CrossRefGoogle Scholar
  77. 77.
    Barry RE, Krek W. The von Hippel-Lindau tumour suppressor: a multi-faceted inhibitor of tumourigenesis. Trends Mol Med. 2004;10(9):466–72.  https://doi.org/10.1016/j.molmed.2004.07.008.CrossRefPubMedGoogle Scholar
  78. 78.
    Richard S, Graff J, Lindau J, Resche F. Von Hippel-Lindau disease. Lancet. 2004;363(9416):1231–4.  https://doi.org/10.1016/S0140-6736(04)15957-6.CrossRefPubMedGoogle Scholar
  79. 79.
    Butman JA, Linehan WM, Lonser RR. Neurologic manifestations of von Hippel-Lindau disease. JAMA. 2008;300(11):1334–42.  https://doi.org/10.1001/jama.300.11.1334.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Maher ER, Neumann HP, Richard S. von Hippel-Lindau disease: a clinical and scientific review. Eur J Hum Genet. 2011;19(6):617–23.  https://doi.org/10.1038/ejhg.2010.175.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Banks RE, Tirukonda P, Taylor C, Hornigold N, Astuti D, Cohen D, Maher ER, Stanley AJ, Harnden P, Joyce A, Knowles M, Selby PJ. Genetic and epigenetic analysis of von Hippel-Lindau (VHL) gene alterations and relationship with clinical variables in sporadic renal cancer. Cancer Res. 2006;66(4):2000–11.  https://doi.org/10.1158/0008-5472.CAN-05-3074.CrossRefPubMedGoogle Scholar
  82. 82.
    Barontini M, Dahia PL. VHL disease. Best Pract Res Clin Endocrinol Metab. 2010;24(3):401–13.  https://doi.org/10.1016/j.beem.2010.01.002.CrossRefPubMedGoogle Scholar
  83. 83.
    Woodward ER, Clifford SC, Astuti D, Affara NA, Maher ER. Familial clear cell renal cell carcinoma (FCRC): clinical features and mutation analysis of the VHL, MET, and CUL2 candidate genes. J Med Genet. 2000;37(5):348–53.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Glasker S. Central nervous system manifestations in VHL: genetics, pathology and clinical phenotypic features. Familial Cancer. 2005;4(1):37–42.  https://doi.org/10.1007/s10689-004-5347-6.CrossRefPubMedGoogle Scholar
  85. 85.
    Glasker S, Bender BU, Apel TW, Natt E, van Velthoven V, Scheremet R, Zentner J, Neumann HP. The impact of molecular genetic analysis of the VHL gene in patients with haemangioblastomas of the central nervous system. J Neurol Neurosurg Psychiatry. 1999;67(6):758–62.PubMedPubMedCentralGoogle Scholar
  86. 86.
    Ridley M, Green J, Johnson G. Retinal angiomatosis: the ocular manifestations of von Hippel-Lindau disease. Can J Ophthalmol. 1986;21(7):276–83.PubMedGoogle Scholar
  87. 87.
    Webster AR, Maher ER, Moore AT. Clinical characteristics of ocular angiomatosis in von Hippel-Lindau disease and correlation with germline mutation. Arch Ophthalmol. 1999;117(3):371–8.PubMedGoogle Scholar
  88. 88.
    Greenwald MJ, Weiss A. Ocular manifestations of the neurocutaneous syndromes. Pediatr Dermatol. 1984;2(2):98–117.PubMedGoogle Scholar
  89. 89.
    Salazar FG, Lamiell JM. Early identification of retinal angiomas in a large kindred von Hippel-Lindau disease. Am J Ophthalmol. 1980;89(4):540–5.PubMedGoogle Scholar
  90. 90.
    Wanebo JE, Lonser RR, Glenn GM, Oldfield EH. The natural history of hemangioblastomas of the central nervous system in patients with von Hippel-Lindau disease. J Neurosurg. 2003;98(1):82–94.  https://doi.org/10.3171/jns.2003.98.1.0082.CrossRefPubMedGoogle Scholar
  91. 91.
    Ammerman JM, Lonser RR, Dambrosia J, Butman JA, Oldfield EH. Long-term natural history of hemangioblastomas in patients with von Hippel-Lindau disease: implications for treatment. J Neurosurg. 2006;105(2):248–55.  https://doi.org/10.3171/jns.2006.105.2.248.CrossRefPubMedGoogle Scholar
  92. 92.
    Hanakita S, Koga T, Shin M, Takayanagi S, Mukasa A, Tago M, Igaki H, Saito N. The long-term outcomes of radiosurgery for intracranial hemangioblastomas. Neuro-Oncology. 2014;16(3):429–33.  https://doi.org/10.1093/neuonc/not201.CrossRefPubMedGoogle Scholar
  93. 93.
    Neumann HP, Bausch B, McWhinney SR, Bender BU, Gimm O, Franke G, Schipper J, Klisch J, Altehoefer C, Zerres K, Januszewicz A, Eng C, Smith WM, Munk R, Manz T, Glaesker S, Apel TW, Treier M, Reineke M, Walz MK, Hoang-Vu C, Brauckhoff M, Klein-Franke A, Klose P, Schmidt H, Maier-Woelfle M, Peczkowska M, Szmigielski C, Eng C, Freiburg-Warsaw-Columbus Pheochromocytoma Study Group. Germ-line mutations in nonsyndromic pheochromocytoma. N Engl J Med. 2002;346(19):1459–66.  https://doi.org/10.1056/NEJMoa020152.CrossRefPubMedGoogle Scholar
  94. 94.
    Steinbach F, Novick AC, Zincke H, Miller DP, Williams RD, Lund G, Skinner DG, Esrig D, Richie JP, deKernion JB, et al. Treatment of renal cell carcinoma in von Hippel-Lindau disease: a multicenter study. J Urol. 1995;153(6):1812–6.PubMedGoogle Scholar
  95. 95.
    Stein PP, Black HR. A simplified diagnostic approach to pheochromocytoma. A review of the literature and report of one institution's experience. Medicine (Baltimore). 1991;70(1):46–66.Google Scholar
  96. 96.
    Sutton MG, Sheps SG, Lie JT. Prevalence of clinically unsuspected pheochromocytoma. Review of a 50-year autopsy series. Mayo Clin Proc. 1981;56(6):354–60.PubMedGoogle Scholar
  97. 97.
    Tsirlin A, Oo Y, Sharma R, Kansara A, Gliwa A, Banerji MA. Pheochromocytoma: a review. Maturitas. 2014;77(3):229–38.  https://doi.org/10.1016/j.maturitas.2013.12.009.CrossRefPubMedGoogle Scholar
  98. 98.
    Neumann HP, Eggert HR, Weigel K, Friedburg H, Wiestler OD, Schollmeyer P. Hemangioblastomas of the central nervous system. A 10-year study with special reference to von Hippel-Lindau syndrome. J Neurosurg. 1989;70(1):24–30.  https://doi.org/10.3171/jns.1989.70.1.0024.CrossRefPubMedGoogle Scholar
  99. 99.
    Chamberlain MC, Tredway TL. Adult primary intradural spinal cord tumors: a review. Curr Neurol Neurosci Rep. 2011;11(3):320–8.  https://doi.org/10.1007/s11910-011-0190-2.CrossRefPubMedGoogle Scholar
  100. 100.
    Baker KB, Moran CJ, Wippold FJ 2nd, Smirniotopoulos JG, Rodriguez FJ, Meyers SP, Siegal TL. MR imaging of spinal hemangioblastoma. AJR Am J Roentgenol. 2000;174(2):377–82.  https://doi.org/10.2214/ajr.174.2.1740377.CrossRefPubMedGoogle Scholar
  101. 101.
    Cristante L, Herrmann HD. Surgical management of intramedullary hemangioblastoma of the spinal cord. Acta Neurochir. 1999;141(4):333–9. discussion 339-340PubMedGoogle Scholar
  102. 102.
    Roonprapunt C, Silvera VM, Setton A, Freed D, Epstein FJ, Jallo GI. Surgical management of isolated hemangioblastomas of the spinal cord. Neurosurgery. 2001;49(2):321–7. discussion 327-328PubMedGoogle Scholar
  103. 103.
    Ohtakara K, Kuga Y, Murao K, Kojima T, Taki W, Waga S. Preoperative embolization of upper cervical cord hemangioblastoma concomitant with venous congestion--case report. Neurol Med Chir (Tokyo). 2000;40(11):589–93.Google Scholar
  104. 104.
    Mandigo CE, Ogden AT, Angevine PD, McCormick PC. Operative management of spinal hemangioblastoma. Neurosurgery. 2009;65(6):1166–77.  https://doi.org/10.1227/01.NEU.0000359306.74674.C4.CrossRefPubMedGoogle Scholar
  105. 105.
    Lonser RR, Weil RJ, Wanebo JE, DeVroom HL, Oldfield EH. Surgical management of spinal cord hemangioblastomas in patients with von Hippel-Lindau disease. J Neurosurg. 2003;98(1):106–16.  https://doi.org/10.3171/jns.2003.98.1.0106.CrossRefPubMedGoogle Scholar
  106. 106.
    Selch MT, Tenn S, Agazaryan N, Lee SP, Gorgulho A, De Salles AA. Image-guided linear accelerator-based spinal radiosurgery for hemangioblastoma. Surg Neurol Int. 2012;3:73.  https://doi.org/10.4103/2152-7806.98386.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Sardi I, Sanzo M, Giordano F, Buccoliero AM, Mussa F, Arico M, Genitori L. Monotherapy with thalidomide for treatment of spinal cord hemangioblastomas in a patient with von Hippel-Lindau disease. Pediatr Blood Cancer. 2009;53(3):464–7.  https://doi.org/10.1002/pbc.22065.CrossRefPubMedGoogle Scholar
  108. 108.
    Madhusudan S, Deplanque G, Braybrooke JP, Cattell E, Taylor M, Price P, Tsaloumas MD, Moore N, Huson SM, Adams C, Frith P, Scigalla P, Harris AL. Antiangiogenic therapy for von Hippel-Lindau disease. JAMA. 2004;291(8):943–4.  https://doi.org/10.1001/jama.291.8.943.CrossRefPubMedGoogle Scholar
  109. 109.
    Hrisomalos FN, Maturi RK, Pata V. Long-term use of intravitreal bevacizumab (avastin) for the treatment of von hippel-lindau associated retinal hemangioblastomas. Open Ophthalmol J. 2010;4:66–9.  https://doi.org/10.2174/1874364101004010066.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Frederick A. Boop
    • 1
    • 2
    • 3
  • Jimmy Ming-Jung Chuang
    • 1
    • 2
    • 4
  • Chenran Zhang
    • 1
    • 2
    • 5
    • 6
  1. 1.Department of NeurosurgeryUniversity of Tennessee Health Science CenterMemphisUSA
  2. 2.Department of NeurosurgeryLe Bonheur Children’s HospitalMemphisUSA
  3. 3.Semmes MurpheyMemphisUSA
  4. 4.Kaohsiung Chang Gung Memorial HospitalKaohsiungTaiwan
  5. 5.Xinhua Hospital, School of Medicine, Shanghai Jiao Tong UniversityShanghaiChina
  6. 6.Changzheng Hospital, Second Military Medical UniversityShanghaiChina

Personalised recommendations