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Neuroradiology

, Volume 48, Issue 10, pp 745–754 | Cite as

Virchow-Robin spaces on magnetic resonance images: normative data, their dilatation, and a review of the literature

  • Samuel GroeschelEmail author
  • Wui Khean Chong
  • Robert Surtees
  • Folker Hanefeld
Paediatric Neuroradiology

Abstract

Introduction

Virchow-Robin spaces (VRS) are perivascular spaces in the brain and can be visualized on magnetic resonance images (MRI). We attempt to provide a better understanding of the significance of VRS for pathological and physiological processes by reviewing the literature, presenting normative data for the first time, and proposing a definition for the dilatation of the VRS on MRI that is based on shape rather than size.

Methods

We evaluated the VRS in 125 healthy subjects (age range 1–30 years) using high-resolution 3D images, and in 36 patients (age range 2–16 years) with normal MRI, using routine clinical sequences.

Results

VRS were visible in all high-resolution images of the 125 healthy subjects. Two of them revealed dilated VRS, giving a prevalence of 1.6%. VRS could be visualized in 29 (80%) of the 36 paediatric clinical scans; none was dilated. It was demonstrated that the visibility of VRS on MRI is sequence-dependent.

Conclusion

From the results of this study and the literature on the nature and pathology of VRS, we conclude that VRS on MR images of healthy individuals are normal findings, even if they are dilated. A judgement on whether dilated VRS in an individual patient is a normal variant or part of a disease process can be made by taking into account the appearance of the adjacent tissue on MRI and the clinical context.

Keywords

Perivascular spaces Virchow-Robin spaces MRI Review 

Notes

Acknowledgements

We thank the Department of Medical Statistics (Prof. Dr. E. Brunner and co-workers) at the Georg-August University, Göttingen, for their statistical advice.

Conflict of interest statement

We declare that we have no conflict of interest.

References

  1. 1.
    Virchow R (1851) Ueber die Erweiterung kleinerer Gefaesse. Arch Pathol Anat Physiol Klin Med 3:427–462CrossRefGoogle Scholar
  2. 2.
    Robin C (1859) Recherches sur quelques particularites de la structure des capillaires de l’encephale. J Physiol Homme Animaux 2:537–548Google Scholar
  3. 3.
    Weller RO (1998) Pathology of cerebrospinal fluid and interstitial fluid of the CNS: significance for Alzheimer disease, prion disorders and multiple sclerosis. J Neuropathol Exp Neurol 57:885–894PubMedGoogle Scholar
  4. 4.
    Weller RO, Kida S, Zhang ET (1992) Pathways of fluid drainage from the brain – morphological aspects and immunological significance in rat and man. Brain Pathol 2:277–284PubMedGoogle Scholar
  5. 5.
    Esiri MM, Gay D (1990) Immunological and neuropathological significance of the Virchow-Robin space. J Neurol Sci 100:3–8PubMedCrossRefGoogle Scholar
  6. 6.
    Abott NJ (2004) Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology. Neurochem Int 45:545–552PubMedCrossRefGoogle Scholar
  7. 7.
    Heier LA, Bauer CJ, Schwartz L, Zimmerman RD, Morgello S, Deck MD (1989) Large Virchow-Robin spaces: MR–clinical correlation. AJNR Am J Neuroradiol 10:929–936PubMedGoogle Scholar
  8. 8.
    Barkhof F (2004) Enlarged Virchow-Robin spaces: do they matter? J Neurol Neurosurg Psychiatry 75:1516–1517PubMedCrossRefGoogle Scholar
  9. 9.
    Frahm J, Haase A, Matthaei D (1986) Rapid three-dimensional MR imaging using the FLASH technique. J Comput Assist Tomogr 10:363–368PubMedGoogle Scholar
  10. 10.
    Maclullich AM, Wardlaw JM, Ferguson KJ, Starr JM, Seckl JR, Deary IJ (2004) Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry 75:1519–1523PubMedCrossRefGoogle Scholar
  11. 11.
    Rollins NK, Deline C, Morriss MC (1993) Prevalence and clinical significance of dilated Virchow-Robin spaces in childhood. Radiology 189:53–57PubMedGoogle Scholar
  12. 12.
    Rafia S, Pizzatto MR, Pascual CI (2001) The importance of the identification of the spaces of Virchow-Robin. A report of four cases. Rev Neurol 33:833–836PubMedGoogle Scholar
  13. 13.
    Jungreis CA, Kanal E, Hirsch WL, Martinez AJ, Moossy J (1988) Normal perivascular spaces mimicking lacunar infarction: MR imaging. Radiology 169:101–104PubMedGoogle Scholar
  14. 14.
    Hirabuki N, Fujita N, Fujii K, Hashimoto T, Kozuka T (1994) MR appearance of Virchow-Robin spaces along lenticulostriate arteries: spin-echo and two-dimensional fast low-angle shot imaging. AJNR Am J Neuroradiol 15:277–281PubMedGoogle Scholar
  15. 15.
    Adachi M, Hosoya T, Haku T, Yamaguchi K (1998) Dilated Virchow-Robin spaces: MRI pathological study. Neuroradiology 40:27–31PubMedCrossRefGoogle Scholar
  16. 16.
    Pollock H, Hutchings M, Weller RO, Zhang ET (1997) Perivascular spaces in the basal ganglia of the human brain: their relationship to lacunes. J Anat 191(Pt 3):337–346PubMedCrossRefGoogle Scholar
  17. 17.
    Bokura H, Kobayashi S, Yamaguchi S (1998) Distinguishing silent lacunar infarction from enlarged Virchow-Robin spaces: a magnetic resonance imaging and pathological study. J Neurol 245:116–122PubMedCrossRefGoogle Scholar
  18. 18.
    Elster AD, Richardson DN (1991) Focal high signal on MR scans of the midbrain caused by enlarged perivascular spaces: MR–pathologic correlation. AJR Am J Roentgenol 156:157–160PubMedGoogle Scholar
  19. 19.
    Benhaiem-Sigaux N, Gray F, Gherardi R, Roucayrol AM, Poirier J (1987) Expanding cerebellar lacunes due to dilatation of the perivascular space associated with Binswanger’s subcortical arteriosclerotic encephalopathy. Stroke 18:1087–1092PubMedGoogle Scholar
  20. 20.
    Song CJ, Kim JH, Kier EL, Bronen RA (2000) MR imaging and histologic features of subinsular bright spots on T2-weighted MR images: Virchow-Robin spaces of the extreme capsule and insular cortex. Radiology 214:671–677PubMedGoogle Scholar
  21. 21.
    Saeki N, Nagai Y, Matsuura I, Uchino Y, Kubota M, Murai H, Ishikura H, Ikehira H, Yamaura A (2004) Histologic characteristics of normal perivascular spaces along the optic tract: new pathogenetic mechanism for edema in tumors in the pituitary region. AJNR Am J Neuroradiol 25:1218–1222PubMedGoogle Scholar
  22. 22.
    Woollam DHM, Millen JW (1954) Perivascular spaces of the mammalian central nervous system. Biol Rev 29:251–283Google Scholar
  23. 23.
    Pestalozzi H (1849) Über Aneurysmata spuria der kleinen Gehirnarterien und ihren Zusammenhang mit Apoplexie. F.E. Thein, Würtzburg (cited in reference 22)Google Scholar
  24. 24.
    His W (1865) Ueber ein perivaskulaeres Kanalsystem in den nervoesen Central-Organen und ueber dessen Beziehungen zum Lymphsystem. Z Wiss Zool 15:127–141Google Scholar
  25. 25.
    Obersteiner H (1870) Über einige Lymphräume im Gehirne. Akad wiss Wien 61:57 (cited in reference 22)Google Scholar
  26. 26.
    Key A, Retzius G (1876) Studien in der Anatomie des Nervensystems und des Bindegewebes. Stockholm (cited in reference 22)Google Scholar
  27. 27.
    Held H (1909) Über die Neuroglia marginalis der menschlichen Grosshirnrinde. Mschr Psychiat Neurol 26:360 (cited in reference 22)CrossRefGoogle Scholar
  28. 28.
    Weed LH (1923) The absorption of cerebrospinal fluid into the nervous system. Am J Anat 31:191–221CrossRefGoogle Scholar
  29. 29.
    Krahn V (1982) The pia mater at the site of the entry of blood vessels into the central nervous system. Anat Embryol (Berl) 164:257–263CrossRefGoogle Scholar
  30. 30.
    Krisch B, Leonhardt H, Oksche A (1984) Compartments and perivascular arrangement of the meninges covering the cerebral cortex of the rat. Cell Tissue Res 238:459–474PubMedCrossRefGoogle Scholar
  31. 31.
    Zhang ET, Inman CB, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:111–123PubMedGoogle Scholar
  32. 32.
    Ozturk MH, Aydingoz U (2002) Comparison of MR signal intensities of cerebral perivascular (Virchow-Robin) and subarachnoid spaces. J Comput Assist Tomogr 26:902–904PubMedCrossRefGoogle Scholar
  33. 33.
    Bradbury MW, Cserr HF, Westrop RJ (1981) Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit. Am J Physiol 240:F329–F336PubMedGoogle Scholar
  34. 34.
    Cserr HF, Harling-Berg CJ, Knopf PM (1992) Drainage of brain extracellular fluid into blood and deep cervical lymph and its immunological significance. Brain Pathol 2:269–276PubMedGoogle Scholar
  35. 35.
    Yamada S, DePasquale M, Patlak CS, Cserr HF (1991) Albumin outflow into deep cervical lymph from different regions of rabbit brain. Am J Physiol 261:H1197–H1204PubMedGoogle Scholar
  36. 36.
    Zhang ET, Richards HK, Kida S, Weller RO (1992) Directional and compartmentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain. Acta Neuropathol (Berl) 83:233–239CrossRefGoogle Scholar
  37. 37.
    Weller RO, Engelhardt B, Phillips MJ (1996) Lymphocyte targeting of the central nervous system: a review of afferent and efferent CNS-immune pathways. Brain Pathol 6:275–288PubMedGoogle Scholar
  38. 38.
    Angelov DN, Walther M, Streppel M, Guntinas-Lichius O, Neiss WF (1998) The cerebral perivascular cells. Adv Anat Embryol Cell Biol 147:1–87PubMedGoogle Scholar
  39. 39.
    McKeever PE, Balentine JD (1978) Macrophages migration through the brain parenchyma to the perivascular space following particle ingestion. Am J Pathol 93:153–164PubMedGoogle Scholar
  40. 40.
    Bechmann I, Priller J, Kovac A, Bontert M, Wehner T, Klett FF, Bohsung J, Stuschke M, Dirnagl U, Nitsch R (2001) Immune surveillance of mouse brain perivascular spaces by blood-borne macrophages. Eur J Neurosci 14:1651–1658PubMedCrossRefGoogle Scholar
  41. 41.
    Bechmann I, Kwidzinski E, Kovac AD, Simburger E, Horvath T, Gimsa U, Dirnagl U, Priller J, Nitsch R (2001) Turnover of rat brain perivascular cells. Exp Neurol 168:242–249PubMedCrossRefGoogle Scholar
  42. 42.
    Hickey WF, Hsu BL, Kimura H (1991) T-lymphocyte entry into the central nervous system. J Neurosci Res 28:254–260PubMedCrossRefGoogle Scholar
  43. 43.
    Silverman AJ, Sutherland AK, Wilhelm M, Silver R (2000) Mast cells migrate from blood to brain. J Neurosci 20:401–408PubMedGoogle Scholar
  44. 44.
    Durand-Fardel M (1843) Traite du ramollissement du cerveau. ParisGoogle Scholar
  45. 45.
    Fisher CM (1998) Lacunes: small, deep cerebral infarcts. 1965. Neurology 50:841PubMedGoogle Scholar
  46. 46.
    Marie P (1901) Des foyers lacunaires de desintegration et de differents autres etats cavitaire du cerveau. Rev Med (Paris) 21:281Google Scholar
  47. 47.
    Fisher CM (1965) Lacunes: small, deep cerebral infarcts. Neurology 15:774–784PubMedGoogle Scholar
  48. 48.
    Poirier J, Derouesne C (1984) Cerebral lacunae. A proposed new classification. Clin Neuropathol 3:266PubMedGoogle Scholar
  49. 49.
    van Swieten JC, van den Hout JH, van Ketel BA, Hijdra A, Wokke JH, van Gijn J (1991) Periventricular lesions in the white matter on magnetic resonance imaging in the elderly. A morphometric correlation with arteriolosclerosis and dilated perivascular spaces. Brain 114(Pt 2):761–774PubMedGoogle Scholar
  50. 50.
    Awad IA, Johnson PC, Spetzler RF, Hodak JA (1986) Incidental subcortical lesions identified on magnetic resonance imaging in the elderly. II. Postmortem pathological correlations. Stroke 17:1090–1097PubMedGoogle Scholar
  51. 51.
    Munoz DG, Hastak SM, Harper B, Lee D, Hachinski VC (1993) Pathologic correlates of increased signals of the centrum ovale on magnetic resonance imaging. Arch Neurol 50:492–497PubMedGoogle Scholar
  52. 52.
    Chimowitz MI, Estes ML, Furlan AJ, Awad IA (1992) Further observations on the pathology of subcortical lesions identified on magnetic resonance imaging. Arch Neurol 49:747–752PubMedGoogle Scholar
  53. 53.
    Scarpelli M, Salvolini U, Diamanti L, Montironi R, Chiaromoni L, Maricotti M (1994) MRI and pathological examination of post-mortem brains: the problem of white matter high signal areas. Neuroradiology 36:393–398PubMedCrossRefGoogle Scholar
  54. 54.
    Kirkpatrick JB, Hayman LA (1987) White-matter lesions in MR imaging of clinically healthy brains of elderly subjects: possible pathologic basis. Radiology 162:509–511PubMedGoogle Scholar
  55. 55.
    Braffman BH, Zimmerman RA, Trojanowski JQ, Gonatas NK, Hickey WF, Schlaepfer WW (1988) Brain MR: pathologic correlation with gross and histopathology. 1. Lacunar infarction and Virchow-Robin spaces. AJR Am J Roentgenol 151:551–558PubMedGoogle Scholar
  56. 56.
    Pullicino PM, Miller LL, Alexandrov AV, Ostrow PT (1995) Infraputaminal ‘lacunes’. Clinical and pathological correlations. Stroke 26:1598–1602PubMedGoogle Scholar
  57. 57.
    Poirier J, Derouesne C (1998) Distinguishing lacunar infarcts from dilatations of the perivascular space. J Neurol 245:813–814PubMedCrossRefGoogle Scholar
  58. 58.
    Cole FM, Yates PO (1968) Comparative incidence of cerebrovascular lesions in normotensive and hypertensive patients. Neurology 18:255–259PubMedCrossRefGoogle Scholar
  59. 59.
    Kertesz A, Black SE, Tokar G, Benke T, Carr T, Nicholson L (1988) Periventricular and subcortical hyperintensities on magnetic resonance imaging. ‘Rims, caps, and unidentified bright objects’. Arch Neurol 45:404–408PubMedGoogle Scholar
  60. 60.
    Erkinjuntti T, Benavente O, Eliasziw M, Munoz DG, Sulkava R, Haltia M, Hachinski V (1996) Diffuse vacuolization (spongiosis) and arteriolosclerosis in the frontal white matter occurs in vascular dementia. Arch Neurol 53:325–332PubMedGoogle Scholar
  61. 61.
    Zimmerman RD, Fleming CA, Lee BC, Saint-Louis LA, Deck MD (1986) Periventricular hyperintensity as seen by magnetic resonance: prevalence and significance. AJR Am J Roentgenol 146:443–450PubMedGoogle Scholar
  62. 62.
    Barkhof F, Scheltens P (2002) Imaging of white matter lesions. Cerebrovasc Dis 13 [Suppl 2]:21–30PubMedCrossRefGoogle Scholar
  63. 63.
    Hughes W (1965) Origin of lacunes. Lancet 2:19–21CrossRefGoogle Scholar
  64. 64.
    Poirier J, Barbizet J, Gaston A, Meyrignac C (1983) Thalamic dementia. Expansive lacunae of the thalamo-paramedian mesencephalic area. Hydrocephalus caused by stenosis of the aqueduct of Sylvius. Rev Neurol (Paris) 139:349–358Google Scholar
  65. 65.
    Homeyer P, Cornu P, Lacomblez L, Chiras J, Derouesne C (1996) A special form of cerebral lacunae: expanding lacunae. J Neurol Neurosurg Psychiatry 61:200–202PubMedGoogle Scholar
  66. 66.
    Vital C, Julien J (1997) Widespread dilatation of perivascular spaces: a leukoencephalopathy causing dementia. Neurology 48:1310–1313PubMedGoogle Scholar
  67. 67.
    Shiratori K, Mrowka M, Toussaint A, Spalke G, Bien S (2002) Extreme, unilateral widening of Virchow-Robin spaces: case report. Neuroradiology 44:990–992PubMedCrossRefGoogle Scholar
  68. 68.
    Ugawa Y, Shirouzu I, Terao Y, Hanajima R, Machii K, Mochizuki H, Furubayashi T, Kanazawa I (1998) Physiological analyses of a patient with extreme widening of Virchow-Robin spaces. J Neurol Sci 159:25–27PubMedCrossRefGoogle Scholar
  69. 69.
    Bacheschi LA, Magalhaes ACA, Mathias SC (1995) Multiple cystic lesions on white matter without clinical manifestations (unidentified black holes). Proceedings of the XV Symposium Neuroradiologicum 37 (supplement), pp 246–247Google Scholar
  70. 70.
    Ogawa T, Okudera T, Fukasawa H, Hashimoto M, Inugami A, Fujita H, Hatazawa J, Shimosegawa E, Noguchi K, Uemura K (1995) Unusual widening of Virchow-Robin spaces: MR appearance. AJNR Am J Neuroradiol 16:1238–1242PubMedGoogle Scholar
  71. 71.
    Demaerel P, Wilms G, Baert AL, Van den Bergh V, Sainte T (1996) Widening of Virchow-Robin spaces. AJNR Am J Neuroradiol 17:800–801PubMedGoogle Scholar
  72. 72.
    Eichhorn GR, Ammache Z, Bell W, Yuh WT (2001) Unusually prominent perivascular spaces. Neurology 56:1242PubMedGoogle Scholar
  73. 73.
    Afifi AK (1996) Enlarged Virchow-Robin spaces along the medullary perforators in a child with seizures. J Neuroimaging 6:197–198PubMedGoogle Scholar
  74. 74.
    Komiyama M, Yasui T, Izumi T (1998) Magnetic resonance imaging features of unusually dilated Virchow-Robin spaces–two case reports. Neurol Med Chir (Tokyo) 38:161–164Google Scholar
  75. 75.
    Romi F, Tysnes OB, Krakenes J, Savoiardo M, Aarli JA, Bindoff L (2002) Cystic dilation of Virchow-Robin spaces in the midbrain. Eur Neurol 47:186–188PubMedCrossRefGoogle Scholar
  76. 76.
    el Quessar A, Brique S, Destee A, Pruvo JP (1999) What is your diagnosis? Unusual dilatation of the Virchow-Robin space. J Radiol 80:951–953PubMedGoogle Scholar
  77. 77.
    Mascalchi M, Salvi F, Godano U, Nistri M, Taiuti R, Tosetti M, Villari N, Calbucci F (1999) Expanding lacunae causing triventricular hydrocephalus. Report of two cases. J Neurosurg 91:669–674PubMedGoogle Scholar
  78. 78.
    Wilkins RH, Burger PC (1988) Benign intraparenchymal brain cysts without an epithelial lining. J Neurosurg 68:378–382PubMedCrossRefGoogle Scholar
  79. 79.
    Cakirer S (2003) MR imaging findings in tumefactive perivascular spaces. Acta Radiol 44:673–674PubMedGoogle Scholar
  80. 80.
    Papayannis CE, Saidon P, Rugilo CA, Hess D, Rodriguez G, Sica RE, Rey RC (2003) Expanding Virchow Robin spaces in the midbrain causing hydrocephalus. AJNR Am J Neuroradiol 24:1399–1403PubMedGoogle Scholar
  81. 81.
    Kanamalla US, Calabro F, Jinkins JR (2000) Cavernous dilatation of mesencephalic Virchow-Robin spaces with obstructive hydrocephalus. Neuroradiology 42:881–884PubMedCrossRefGoogle Scholar
  82. 82.
    Afifi AK, Sato Y, Waziri MH, Bell WE (1990) Computed tomography and magnetic resonance imaging of the brain in Hurler’s disease. J Child Neurol 5:235–241PubMedGoogle Scholar
  83. 83.
    Barone R, Nigro F, Triulzi F, Musumeci S, Fiumara A, Pavone L (1999) Clinical and neuroradiological follow-up in mucopolysaccharidosis type III (Sanfilippo syndrome). Neuropediatrics 30:270–274PubMedGoogle Scholar
  84. 84.
    Gabrielli O, Salvolini U, Maricotti M, Mariani MG, Coppa GV, Giorgi PL (1992) Cerebral MRI in two brothers with mucopolysaccharidosis type I and different clinical phenotypes. Neuroradiology 34:313–315PubMedCrossRefGoogle Scholar
  85. 85.
    Lee C, Dineen TE, Brack M, Kirsch JE, Runge VM (1993) The mucopolysaccharidoses: characterization by cranial MR imaging. AJNR Am J Neuroradiol 14:1285–1292PubMedGoogle Scholar
  86. 86.
    Matheus MG, Castillo M, Smith JK, Armao D, Towle D, Muenzer J (2004) Brain MRI findings in patients with mucopolysaccharidosis types I and II and mild clinical presentation. Neuroradiology 46:666–672PubMedCrossRefGoogle Scholar
  87. 87.
    Murata R, Nakajima S, Tanaka A, Miyagi N, Matsuoka O, Kogame S, Inoue Y (1989) MR imaging of the brain in patients with mucopolysaccharidosis. AJNR Am J Neuroradiol 10:1165–1170PubMedGoogle Scholar
  88. 88.
    Parsons VJ, Hughes DG, Wraith JE (1996) Magnetic resonance imaging of the brain, neck and cervical spine in mild Hunter’s syndrome (mucopolysaccharidoses type II). Clin Radiol 51:719–723PubMedCrossRefGoogle Scholar
  89. 89.
    Shimoda-Matsubayashi S, Kuru Y, Sumie H, Ito T, Hattori N, Okuma Y, Mizuno Y (1990) MRI findings in the mild type of mucopolysaccharidosis II (Hunter’s syndrome). Neuroradiology 32:328–330PubMedCrossRefGoogle Scholar
  90. 90.
    Barkovich AJ (1999) Pediatric neuroimaging. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  91. 91.
    Van der Knaap MS, Valk J (1995) Magnetic resonance of myelin, myelination and myelin disorders. Springer, Berlin Heidelberg New YorkGoogle Scholar
  92. 92.
    Patlas M, Shapira MY, Nagler A, Sheffer R, Gomori JM (2001) MRI of mannosidosis. Neuroradiology 43:941–943PubMedCrossRefGoogle Scholar
  93. 93.
    Di Costanzo A, Di Salle F, Santoro L, Tessitore A, Bonavita V, Tedeschi G (2002) Pattern and significance of white matter abnormalities in myotonic dystrophy type 1: an MRI study. J Neurol 249:1175–1182PubMedCrossRefGoogle Scholar
  94. 94.
    Di Costanzo A, Di Salle F, Santoro L, Bonavita V, Tedeschi G (2001) Dilated Virchow-Robin spaces in myotonic dystrophy: frequency, extent and significance. Eur Neurol 46:131–139PubMedCrossRefGoogle Scholar
  95. 95.
    Kondoh T, Matsumoto T, Ochi M, Sukegawa K, Tsuji Y (1998) New radiological finding by magnetic resonance imaging examination of the brain in Coffin-Lowry syndrome. J Hum Genet 43:59–61PubMedCrossRefGoogle Scholar
  96. 96.
    Patlas M, Joseph A, Cohen JE, Gomori JM (2003) MRI and MRS of Coffin-Lowry syndrome: a case report. Neurol Res 25:285–286PubMedCrossRefGoogle Scholar
  97. 97.
    Coulthard A, Blank SC, Bushby K, Kalaria RN, Burn DJ (2000) Distribution of cranial MRI abnormalities in patients with symptomatic and subclinical CADASIL. Br J Radiol 73:256–265PubMedGoogle Scholar
  98. 98.
    Cumurciuc R, Guichard JP, Reizine D, Gray F, Bousser MG, Chabriat H (2006) Dilation of Virchow-Robin spaces in CADASIL. Eur J Neurol 13:187–190PubMedCrossRefGoogle Scholar
  99. 99.
    Baudrimont M, Dubas F, Joutel A, Tournier-Lasserve E, Bousser MG (1993) Autosomal dominant leukoencephalopathy and subcortical ischemic stroke. A clinicopathological study. Stroke 24:122–125PubMedGoogle Scholar
  100. 100.
    Vahedi K, Massin P, Guichard JP, Miocque S, Polivka M, Goutieres F, Dress D, Chapon F, Ruchoux MM, Riant F, Joutel A, Gaudric A, Bousser MG, Tournier-Lasserve E (2003) Hereditary infantile hemiparesis, retinal arteriolar tortuosity, and leukoencephalopathy. Neurology 60:57–63PubMedGoogle Scholar
  101. 101.
    Patankar TF, Mitra D, Varma A, Snowden J, Neary D, Jackson A (2005) Dilatation of the Virchow-Robin space is a sensitive indicator of cerebral microvascular disease: study in elderly patients with dementia. AJNR Am J Neuroradiol 26:1512–1520PubMedGoogle Scholar
  102. 102.
    Schick S, Gahleitner A, Wober-Bingol C, Wober C, Ba-Ssalamah A, Schoder M, Schindler E, Prayer D (1999) Virchow-Robin spaces in childhood migraine. Neuroradiology 41:283–287PubMedCrossRefGoogle Scholar
  103. 103.
    Sener RN (1994) Polycystic brain (cerebrum polycystica vera) associated with ectodermal dysplasia: a new neurocutaneous syndrome. Pediatr Radiol 24:116–118PubMedCrossRefGoogle Scholar
  104. 104.
    Di Fazio MP, Levin S, Depper M (2002) Ectodermal dysplasia and brain cystic changes: confirmation of a novel neurocutaneous syndrome. J Child Neurol 17:475–478Google Scholar
  105. 105.
    Lynch SA, Hall K, Precious S, Wilkies AO, Hurst JA (2000) Two further cases of Sener syndrome: frontonasal dysplasia and dilated Virchow-Robin spaces. J Med Genet 37:466–470PubMedCrossRefGoogle Scholar
  106. 106.
    Sener RN (1998) A patient with ectodermal dysplasia, Joubert’s syndrome, and brain cysts. Comput Med Imaging Graph 22:349–351PubMedCrossRefGoogle Scholar
  107. 107.
    Vaquerizo-Madrid J, Gamero-Telo JL, Caceres-Marzal C, Escobar-Bejarano M, Fernandez-Calderon E (2004) Hair with a double crown and dilatation of Virchow-Robin spaces: a proposal for a new neurocutaneous association. Rev Neurol 39:350–353PubMedGoogle Scholar
  108. 108.
    Mirfakhraee M, Crofford MJ, Guinto FC Jr, Nauta HJ, Weedn VW (1986) Virchow-Robin space: a path of spread in neurosarcoidosis. Radiology 158:715–720PubMedGoogle Scholar
  109. 109.
    Sherman JL, Stern BJ (1990) Sarcoidosis of the CNS: comparison of unenhanced and enhanced MR images. AJNR Am J Neuroradiol 11:915–923PubMedGoogle Scholar
  110. 110.
    Cheng YC, Ling JF, Chang FC, Wang SJ, Fuh JL, Chen SS, Teng MM, Chang CY (2003) Radiological manifestations of cryptococcal infection in central nervous system. J Chin Med Assoc 66:19–26PubMedCrossRefGoogle Scholar
  111. 111.
    Ueda H, Toribe Y, Kuwae Y, Takeuchi M, Nakayama M, Ida S, Okamoto N, Suzuki Y (2003) An autopsy case of cryptococcal meningoencephalitis: correlation of MRI and pathologic findings. No To Hattatsu 35:499–504PubMedGoogle Scholar
  112. 112.
    Miszkiel KA, Hall-Craggs MA, Miller RF, Kendall BE, Wilkinson ID, Paley MN, Harrison MJ (1996) The spectrum of MRI findings in CNS cryptococcosis in AIDS. Clin Radiol 51:842–850PubMedCrossRefGoogle Scholar
  113. 113.
    Miyakawa T, Hattori E, Shikai I, Shimoji A, Nagatoshi K (1977) Histopathological changes of chronic alcoholism. Folia Psychiatr Neurol Jpn 31:253–261PubMedGoogle Scholar
  114. 114.
    Fenelon G, Gray F, Wallays C, Poirier J, Guillard A (1995) Parkinsonism and dilatation of the perivascular spaces (etat crible) of the striatum: a clinical, magnetic resonance imaging, and pathological study. Mov Disord 10:754–760PubMedCrossRefGoogle Scholar
  115. 115.
    Taber KH, Shaw JB, Loveland KA, Pearson DA, Lane DM, Hayman LA (2004) Accentuated Virchow-Robin spaces in the centrum semiovale in children with autistic disorder. J Comput Assist Tomogr 28:263–268PubMedCrossRefGoogle Scholar
  116. 116.
    Hanefeld F, Riehm H (1980) Therapy of acute lymphoblastic leukaemia in childhood: effects on the nervous system. Neuropadiatrie 11:3–16PubMedCrossRefGoogle Scholar
  117. 117.
    Artigas J, Poo P, Rovira A, Cardo E (1999) Macrocephaly and dilated Virchow-Robin spaces in childhood. Pediatr Radiol 29:188–190PubMedCrossRefGoogle Scholar
  118. 118.
    Groeschel S, Brockmann K, Dechent P, Wilichowski E, Frahm J, Hanefeld F (2006) Magnetic resonance imaging and proton magnetic resonance spectroscopy of megalencephaly and dilated Virchow-Robin spaces. Pediatr Neurol 34:35–40PubMedCrossRefGoogle Scholar
  119. 119.
    Hartel C, Bachmann S, Bonnemann C, Meinecke P, Sperner J (2005) Familial megalencephaly with dilated Virchow-Robin spaces in magnetic resonance imaging: an autosomal recessive trait? Clin Dysmorphol 14:31–34PubMedCrossRefGoogle Scholar
  120. 120.
    Achiron A, Faibel M (2002) Sandlike appearance of Virchow-Robin spaces in early multiple sclerosis: a novel neuroradiologic marker. AJNR Am J Neuroradiol 23:376–380PubMedGoogle Scholar
  121. 121.
    Inglese M, Bomsztyk E, Gonen O, Mannon LJ, Grossman RI, Rusinek H (2005) Dilated perivascular spaces: hallmarks of mild traumatic brain injury. AJNR Am J Neuroradiol 26:719–724PubMedGoogle Scholar
  122. 122.
    Kanpittaya J, Jitpimolmard S, Tiamkao S, Mairiang E (2000) MR findings of eosinophilic meningoencephalitis attributed to Angiostrongylus cantonensis. AJNR Am J Neuroradiol 21:1090–1094PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Samuel Groeschel
    • 1
    • 4
    Email author
  • Wui Khean Chong
    • 2
  • Robert Surtees
    • 3
  • Folker Hanefeld
    • 1
  1. 1.Department of Pediatrics and Child NeurologyGeorg-August-UniversityGoettingenGermany
  2. 2.Radiology and Physics Unit, Institute of Child HealthUniversity College LondonLondonUK
  3. 3.Neurosciences Unit, Institute of Child HealthUniversity College LondonLondonUK
  4. 4.Department of Pediatrics and NeuropediatricsChildren’s HospitalGoettingenGermany

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