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MR assessment of pediatric hydrocephalus: a road map

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Abstract

Purpose

This study was conducted to design a rational approach to the MR diagnosis of hydrocephalus based on a pathophysiologic reevaluation of its possible mechanisms and to apply it to the different etiological contexts.

Method

A review of the literature reports describing new physiologic models of production and absorption and of the hydrodynamics of the CSF was made.

Results

Besides the secretion of CSF by the choroid plexuses, and its passive, pressure-dependent transdural absorption (arachnoid villi, dural clefts, cranial, and spinal nerve sheaths), water transporters, aquaporins, allow water (if not ions and organic molecules) to exchange freely between the brain parenchyma and the CSF spaces across the ependymal and the pial interfaces (including the Virchow-Robin spaces). Consequently, the CSF bulk flow is not necessarily global, and situations of balanced absorption-secretion may occur separately in different CSF compartments such as the ventricular, intracranial, or intraspinal CSF spaces. This means that rather than from a hypothetical pressure gradient from the plexuses to the dural sinuses, the dynamics of the CSF depend on the force provided in those different compartments by the arterial systolic pulsation of the pericerebral (mostly), intracerebral, and intraventricular (choroid plexuses) vascular beds.

Conclusion

Using MR imaging, diverse varieties of hydrocephalus may tentatively be explained by applying those concepts to the correspondingly diverse causal diseases. Hopefully, this may have an impact on the choice of the treatment strategies also.

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Abbreviations

ANP:

Atrial natriuretic peptide

AS:

Aqueductal stenosis

CBF:

Cerebral blood flow

CSF:

Cerebrospinal fluid

GA:

Gestational age

HIE:

Hypoxic-ischemic encephalopathy

ICP:

Intracranial pressure

ISF:

Interstitial fluid

IVH:

Intraventricular hemorrhage

MMC:

Myelomeningocele

NPH:

Normal pressure hydrocephalus

PVHI:

Periventricular hemorrhagic infarction

PVS:

Perivascular space

PVL:

Periventricular leucomalacia

PWML:

Punctate white matter lesion

VRS:

Virchow-Robin space

References

  1. Agre P, Preston GM, Smith BL et al (1993) Aquaporin CHIP: the archetypal molecular water channel. Am J Physiol 34:F463–F476

    Google Scholar 

  2. Ahrensen JT, Macklin W (2013) Signaling mechanisms regulating myelination in the central nervous system. Neurosci Bull 29:199–215

    Article  CAS  Google Scholar 

  3. Akbik F, Cafferty WB, Strittmatter SM (2012) Myelin associated inhibitors: a link between injury-induced and experience-dependent plasticity. Exp Neurol 235:43–52

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Alcolado R, Weller RO, Parrish EP, Garrod D (1988) The cranial arachnoid and pia mater in man: anatomical and ultrastructural observations. Neuropathol Appl Neurobiol 14:1–17

    Article  CAS  PubMed  Google Scholar 

  5. Algin O, Turkbey B (2012) Evaluation of aqueductal stenosis by 3D sampling perfection with application-optimized contrasts using different flip angle evolutions sequence: preliminary results with 3T MR imaging. AJNR Am J Neuroradiol 33(4):740–746

    Article  CAS  PubMed  Google Scholar 

  6. Alperin NJ, Lee SH, Loth F et al (2000) MR-intracranial pressure (ICP): a method to measure intracranial elastance and pressure non-invasively by means of MR imaging. Baboon and human study. Radiology 217:877–885

    Article  CAS  PubMed  Google Scholar 

  7. Andresen M, Juhler M (2012) Multiloculated hydrocephalus: a review of current problems in classification and treatment. Childs Nerv Syst 28:357–362

    Article  PubMed  Google Scholar 

  8. Arichi T, Counsell SJ, Allievi AG et al (2014) The effects of hemorrhagic parenchymal infarction on the establishment of sensori-motor structural and functional connectivity in early infancy. Neuroradiology 56:985–994

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Artru AA (1999) Spinal cerebrospinal fluid chemistry and physiology. In: Yaksh TL (ed) Spinal drug delivery. Elsevier, Amsterdam, pp 177–238

    Google Scholar 

  10. Assaf Y, Ben-Sira L, Constantini S et al (2006) Diffusion tensor imaging in hydrocephalus: initial experience. AJNR Am J Neuroradiol 27:1717–1724

    CAS  PubMed  Google Scholar 

  11. Aziz AA, Coleman L, Morokoff A, Maixner W (2005) Diffuse choroid plexus hyperplasia: an under-diagnosed cause of hydrocephalus in children? Pediatr Radiol 35:815–818

    Article  PubMed  Google Scholar 

  12. Badaut J, Lasbennes F, Magistretti PJ, Regli L (2002) Aquaporins in brain: distribution, physiology and pathophysiology. J Cereb Bllod Flow Metab 22:367–378

    Article  CAS  Google Scholar 

  13. Banizs B, Pike MM, Millican CL et al (2005) Dysfunctional cilia lead to altered ependyma and choroid plexus function, and results in the formation of hydrocephalus. Devel Dis 132:5329–5339

    CAS  Google Scholar 

  14. Bateman GA, Smith RL, Siddique SH (2007) Idiopathic hydrocephalus in children and idiopathic intracranial hypertension in adults: two manifestations of the same physiopathological process? Neurosurgery 107(6 Suppl Pediatrics):439–444

    Google Scholar 

  15. Benarroch EE (2011) Circumventricular organs. Receptive and homeostatic functions and clinical implications. Neurology 77:1198–1204

    Article  PubMed  Google Scholar 

  16. Beni-Adani L, Biani N, Ben-Sirah L, Constantini S (2006) The occurrence of obstructive vs absorptive hydrocephalus in newborns and infants: relevance to treatment choices. Childs Nerv Syst 22:1543–1563

    Article  PubMed  Google Scholar 

  17. Bergsneider M, Egnor MR, Johnston M et al (2006) What we don’t (but should) know about hydrocephalus. J Neurosurg 104(3 Suppl Pediatrics):157–159

    PubMed  Google Scholar 

  18. Bering EA (1952) Water exchange of central nervous system and cerebrospinal fluid. J Neurosurg 9:275–287

    Article  PubMed  Google Scholar 

  19. Bering EA (1954) Water exchange in the brain and cerebrospinal fluid. J Neurosurg 11:234–242

    Article  CAS  PubMed  Google Scholar 

  20. Bering EA (1955) Choroid plexus and arterial pulsation of cerebrospinal fluid. Demonstration of the choroid plexuses as a cerebrospinal fluid pump. AMA Arch Neurol Neurosurg Chicago 73:165–172

    Google Scholar 

  21. Bering EA (1962) Circulation of the cerebrospinal fluid. Demonstration of the choroid plexuses as the generator of the force for flow of fluid and ventricular enlargement. J Neurosurg 19:405–413

    Article  PubMed  Google Scholar 

  22. Bering EA, Sato O (1963) Hydrocephalus: changes in formation and absorption of cerebrospinal fluid within the cerebral ventricles. J Neurosurg 20:1050–1063

    Article  PubMed  Google Scholar 

  23. Blake JA (1900) The roof and lateral recesses of the fourth ventricle, considered morphologically and embryologically. J Comp Neurol 10:79–108

    Article  Google Scholar 

  24. Bondy C, Chin E, Smith BL et al (1993) Developmental gene expression and tissue distribution of the CHIP28 water-channel protein. Proc Natl Acad Sci U S A 90:4500–4504

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Bozanovic-Sosic R, Mollanji R, Johnston MG (2001) Spinal and cranial contribution to total cerebrospinal fluid transport. Am J Physiol Regul Integr Comp Physiol 281:R909–R916

    CAS  PubMed  Google Scholar 

  26. Bradley WG, Kortman KE, Burgoyne B (1986) Flowing cerebrospinal fluid in normal and hydrocephalic states: appearance on MR images. Radiology 159(3):611–616

    Article  PubMed  Google Scholar 

  27. Bradley WG, Whitemore AR, Kortman KE et al (1991) Marked cerebrospinal fluid void: indicator of successful shunt in patients with suspected normal-pressure hydrocephalus. Radiology 178:459–466

    Article  PubMed  Google Scholar 

  28. Bradley WG (2015) CSF flow in the brain in the context of normal pressure hydrocephalus. AJNR Am J Neuroradiol 36:831–838

    Article  PubMed  Google Scholar 

  29. Braun KPJ, Gooskens RHJM, Vandertop WP et al (2003) 1H magnetic resonance spectroscopy in human hydrocephalus. J Magn Reson Imag 17:291–299

    Article  Google Scholar 

  30. Brinker T, Stopa E, Morrison J, Klinge P (2014) A new look at cerebrospinal fluid circulation. Fluids Barriers CNS 11:10

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  31. Brocklehurst G (1969) The development of the cerebrospinal fluid pathway with particular reference to the roof of the fourth ventricle. J Anat 105:467–475

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Brodbelt A, Stoodley M (2007) CSF pathways: a review. Brit J Neurosurg 21:510–520

    Article  CAS  Google Scholar 

  33. Bulat M, Lupret V, Orešković D, Klarica M (2008) Transventricular and transpial absorption of cerebrospinal fluid into cerebral microvessels. Coll Anthropol 32(Suppl 1):43–50

    Google Scholar 

  34. Bulat M, Klarica M (2011) Recent insights into a new hydrodynamics of the cerebrospinal fluid. Review Brain Res Rev 65:99–112

    Article  PubMed  Google Scholar 

  35. Bystron I, Blakemore C, Rakic P (2008) Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9:110–122

    Article  CAS  PubMed  Google Scholar 

  36. Cardoso ER, Rowan JO, Galbraith S (1983) Analysis of the cerebrospinal pulse wave in intracranial pressure. J Neurosurg 59:817–821

    Article  CAS  PubMed  Google Scholar 

  37. Carrera E, Kim DJ, Castellani G et al (2010) What shapes pulse amplitude of intracranial pressure? J Neurotrauma 27:317–324

    Article  PubMed  Google Scholar 

  38. Castañeyra-Perdomo A, Meyer G, Carmona-Calero E et al (1994) Alterations of the subcommissural organ in the human fetal brain. Devel Brain Res 79:316–320

    Article  Google Scholar 

  39. Catala M (2007) Carbonic anhydrase activity during development of the choroid plexus in the human fetus. Childs Nerv Syst 13:364–368

    Article  Google Scholar 

  40. Cavalheiro S, Moron AF, Zymberg ST, Dastoli P (2003) Fetal hydrocephalus—prenatal treatment. Childs Nerv Syst 19:561–573

    Article  PubMed  Google Scholar 

  41. Chang CC, Kuwana N, Ito S, Ikegami T (1999) Prediction of effectiveness of shunting in patients with normal pressure hydrocephalus by cerebral blood flow measurement and computed tomography cisternography. Neurol Med Chir (Tokyo) 39:845–846

    Article  Google Scholar 

  42. Chauhan SP, Scardo JA, Hayes E et al (2010) Twins: prevalence, problems, and preterm births. Am J Obstet Gynecol 203:305–315

    Article  PubMed  Google Scholar 

  43. Cinalli G, Spennato P, Nastro A et al (2011) Hydrocephalus in aqueductal stenosis. Childs Nerv Syst 27:1621–1642

    Article  PubMed  Google Scholar 

  44. Citrin CM, Sherman JL, Gangarosa RE, Scanlon D (1986) Physiology of the CSF flow void sign: modification by cardiac gating. AJNR Am J Neuroradiol 7:1021–1024

    Google Scholar 

  45. Connor SEJ, O’Gorman R, Summers P et al (2001) SPAMM, cine phase contrast imaging and fast spin-echo T2-weighted imaging in the study of intracranial cerebrospinal fluid flow. Clin Radiol 56:763–772

    Article  CAS  PubMed  Google Scholar 

  46. 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 2:269–276

    Article  CAS  PubMed  Google Scholar 

  47. Cutler RWP, Page L, Galicich G, Watters GV (1968) Formation and absorption of cerebrospinal fluid in man. Brain 91:707–720

    Article  CAS  PubMed  Google Scholar 

  48. Dandy WE, Blackfan KD (1914) Internal hydrocephalus. An experimental, clinical and pathological study. Am J Dis Child 8:406–482

    Article  Google Scholar 

  49. Del Bigio MR (1993) Neuropathological changes caused by hydrocephalus. Acta Neuropathol 85:573–585

    Article  PubMed  Google Scholar 

  50. Del Bigio MR, Zhang YW (1998) Cell death, axonal damage, and cell birth in the immature rat brain following induction of hydrocephalus. Exp Neurol 154:157–169

    Article  PubMed  Google Scholar 

  51. Del Bigio MR, Wilson MJ, Enno T (2003) Chronic hydrocephalus in rats and humans: white matter loss and behavior changes. Ann Neurol 53:337–346

    Article  PubMed  Google Scholar 

  52. Del Bigio MR (2010) Ependymal cells: biology and pathology. Acta Neuropathol 119:55–73

    Article  PubMed  Google Scholar 

  53. Del Bigio MR (2011) Cell proliferation in human ganglionic eminence and suppression after prematurity-associated haemorrhage. Brain 134:1344–1361

    Article  PubMed  Google Scholar 

  54. Demerens C, Stankoff B, Logak M et al (1996) Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci U S A 93:9887–9892

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Desmond ME, Jacobson AG (1977) Embryonic brain enlargement requires cerebrospinal fluid pressure. Dev Biol 57:188–198

    Article  CAS  PubMed  Google Scholar 

  56. De Wit OA, den Dunnen WFA, Sollie KM et al (2008) Pathogenesis of cerebral malformations in human fetuses with myelomeningocele. Cerebrospinal Fluid Res 24:563–575

    Google Scholar 

  57. Dinçer A, Kohan S, Özek MM (2009) Is all “communicating” hydrocephalus really communicating? Prospective study on the value of 3D-constructive interference in steady-state sequence at 3T. AJNR Am J Neuroradiol 30(10):1898–1906

    Article  PubMed  Google Scholar 

  58. Di Rocco C, Pettorossi VE, Caldarelli M et al (1978) Communicating hydrocephalus induced by mechanically increased amplitude of the intraventricular cerebrospinal fluid pressure: experimental studies. Exp Neurol 59:40–52

    Article  PubMed  Google Scholar 

  59. Dominguez-Pinos MD, Páez P, Jiménez AJ et al (2005) Ependymal denudation and alterations of the subependymal zone occur in human fetuses with a moderate communicating hydrocephalus. J Neuropathol Exp Neurol 64:595–604

    Article  PubMed  Google Scholar 

  60. Dziegielewska KM, Ek J, Habgood MD, Saunders NR (2001) Development of the choroid plexus. Microsc Res Tech 52:5–20

    Article  CAS  PubMed  Google Scholar 

  61. Egnor M, Zheng L, Rosiello A et al (2002) A model of pulsations in communicating hydrocephalus. Pediatr Neurosurg 36:281–303

    Article  PubMed  Google Scholar 

  62. Ehrlich S, McComb JG, Hyman S, Weiss MH (1989) Ultrastructure of the orbital pathway for cerebrospinal fluid drainage in rabbits. J Neurosurg 70:926–931

    Article  Google Scholar 

  63. Enzmann DR, Pelc NJ (1993) Cerebrospinal fluid flow measured by phase-contrast cine MR. AJNR Am J Neuroradiol 14:1301–1307

    CAS  PubMed  Google Scholar 

  64. Ferland RJ, Batiz LF, Neal J et al (2009) Disruption of neural progenitors along the ventricular and subventricular zones in periventricular heterotopia. Hum Mol Genet 18:497–516

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  65. Fletcher JM, McCauley SR, Brandt ME et al (1996) Regional brain tissue composition in children with hydrocephalus: relationships with cognitive development. Arch Neurol 53:549–557

    Article  CAS  PubMed  Google Scholar 

  66. Folz EL, Aine C (1981) Diagnosis of hydrocephalus by CSF pulse-wave analysis: a clinical study. Surg Neurol 15:283–293

    Article  Google Scholar 

  67. Fox RJ, Walji AH, Mielke B et al (1996) Anatomic details of intradural channels in the parasagittal dura: a possible pathway for flow of cerebrospinal fluid. Neurosurgery 39:84–91

    Article  CAS  PubMed  Google Scholar 

  68. Galarza M (2002) Evidence of the subcommissural organ in humans and its association with hydrocephalus. Neurosurg Rev 25:205–215

    Article  PubMed  Google Scholar 

  69. Girard NJ, Raybaud CA (2001) Ventriculomegaly and pericerebral CSF collection in the fetus: early stage of benign external hydrocephalus? Childs Nerv Syst 17:239–245

    Article  CAS  PubMed  Google Scholar 

  70. Greitz D, Franck A, Nordell B (1993) On the pulsatile nature of the intracranial and spinal CSF-circulation demonstrated by MR imaging. Acta Radiol 34:321–328

    Article  CAS  PubMed  Google Scholar 

  71. Greitz D (2004) Radiological assessment of hydrocephalus: new theories and implications for therapy. Neurosurg Rev 27:145–165

    PubMed  Google Scholar 

  72. Guirao B, Meunier A, Mortaud S et al (2010) Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat Cell Biol 12:341–350

    Article  CAS  PubMed  Google Scholar 

  73. Guzzetta A, D’Acunto G, Rose S et al (2010) Plasticity of the visual system after early brain damage. Dev Med Child Neurol 52:891–900

    Article  PubMed  Google Scholar 

  74. Hamilton R, Baldwin K, Fuller J et al (2012) Intracranial pressure waveform correlates with aqueductal cerebrospinal fluid stroke volume. J Appl Physiol 113:1560–1566

    Article  PubMed Central  PubMed  Google Scholar 

  75. Hirai O, Handa H, Ishikawa M (1984) Epidural pulse waveform as an indicator of intracranial pressure dynamics. Surg Neurol 21:67–74

    Article  CAS  PubMed  Google Scholar 

  76. Hladky SB, Barrand MA (2014) Mechanisms of fluid movement into, through, and out of the brain: evaluation of the evidence. Fluids Barr CNS 11:26

    Article  Google Scholar 

  77. Hoffmann KT, Lehmann TN, Baumann C, Felix R (2003) CSF flow imaging in the management of third ventriculostomy with a reversed fast imaging with steady-state precession sequence. Eur Radiol 13:1432–1437

    PubMed  Google Scholar 

  78. Hu X, Glenn T, Scalzo F et al (2010) Intracranial pressure pulse morphological features improved detection of decreased cerebral blood flow. Physiol Meas 31:679–695

    Article  PubMed Central  PubMed  Google Scholar 

  79. Iliff JJ, Wang M, Liao Y et al (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 4(147):147ra111

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  80. Illif JJ, Wang M, Zeppenfeld DM et al (2013) Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J Neurosci 33:18190–18199

    Article  CAS  Google Scholar 

  81. Inoue K, Seker A, Ozawa S et al (2009) Microsurgical and endoscopic anatomy of the supratentorial arachnoidal membranes and cisterns. Neurosurgery 65:644–664

    Article  PubMed  Google Scholar 

  82. Jack CR, Mokri B, Laws ER Jr et al (1987) MR findings in normal-pressure hydrocephalus: significance and comparison with other forms of dementia. J Comput Assist Tomogr 11:923–931

    Article  PubMed  Google Scholar 

  83. Jiménez AJ, Tomé M, Páez P et al (2001) A programmed ependymal denudation precedes congenital hydrocephalus in the hyh mutant mouse. J Neuropathol Exp Neurol 60:1105–1119

    Article  PubMed  Google Scholar 

  84. Jimenez AJ, Dominguez-Pinos MD, Guerra MM et al (2014) Structure and function of the ependymal barrier and diseases associated with ependymal disruption. Tissue Barriers 2:228426

    Article  Google Scholar 

  85. Johanson CE, Duncan JA, Klinge P et al (2008) Multiplicity of cerebrospinal fluid functions: new challenges in health and disease. Cerebrospinal Fluid Res 5:10

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  86. Johanson C, Stopa E, McMillan P et al (2011) The distributional nexus of choroid plexus to cerebrospinal fluid, ependyma and brain: toxicologic/pathologic phenomena, periventricular destabilization, and lesion spread. Toxicol Pathol 39:186–212

    Article  PubMed  Google Scholar 

  87. Johansson PA (2014) The choroid plexuses and their impact on developmental neurogenesis. Front Neurosci 8:340

    Article  PubMed Central  PubMed  Google Scholar 

  88. Johnston M, Zakharov A, Papaiconomou et al (2004) Evidence of connections between cerebrospinal fluid and nasal lymphatic vessels in humans, non-human primates and other mammalian species. Cerebrospinal Fluid Res 1:2

    Article  PubMed Central  PubMed  Google Scholar 

  89. Johnston M, Armstrong D, Koh L (2007) Possible role of the cavernous sinus veins in cerebrospinal fluid absorption. Cerebrospinal Fluid Res 4:3

    Article  PubMed Central  PubMed  Google Scholar 

  90. Jung JS, Bhat RV, Preston GM et al (1994) Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci 91:13052–13056

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  91. Kehrer M, Blumenstock G, Ehehalt S et al (2005) Development of the cerebral blood flow volume in preterm neonates during the first two weeks of life. Pediatr Res 58:927–930

    Article  PubMed  Google Scholar 

  92. Kendall B, Holland I (1981) Benign communicating hydrocephalus in children. Neuroradiology 21:93–96

    Article  CAS  PubMed  Google Scholar 

  93. Klarica M, Orešković D, Božić B et al (2009) New experimental model of acute aqueductal blockage in cats: effects on cerebrospinal fluid pressure and the size of brain ventricles. Neuroscience 158:1397–1405

    Article  CAS  PubMed  Google Scholar 

  94. Klosovskii BN (1963) The development of the brain and its disturbance by harmful factors. Pergamon, London

    Google Scholar 

  95. Kostovic I, Judas M, Rados M, Hradac P (2002) Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 12:536–544

    Article  PubMed  Google Scholar 

  96. Kuban KC, Gilles FH (1985) Human telencephalic angiogenesis. Ann Neurol 17:539–548

    Article  CAS  PubMed  Google Scholar 

  97. Laitt RD, Mallucci CL, Jaspan T et al (1999) Constructive interference in steady state 3D Fourier-transform MRI in the management of hydrocephalus and third ventriculostomy. Neuroradiology 41:117–123

    Article  CAS  PubMed  Google Scholar 

  98. Larsson A, Moonen M, Bergh AC et al (1990) Predictive value of quantitative cisternography in normal pressure hydrocephalus. Acta Neurol Scand 81:327–332

    Article  CAS  PubMed  Google Scholar 

  99. Laurence KM (1979) The biology of choroid plexus papilloma in infancy and childhood. Acta Neurochir 50:79–90

    Article  CAS  PubMed  Google Scholar 

  100. Lee L (2013) Riding the wave of ependymal cilia: genetic susceptibility to hydrocephalus in primary ciliary dyskinesia. J Neurosci Res 91:1117–1132

    Article  CAS  PubMed  Google Scholar 

  101. Leliefeld PH, Gooskens RHJM, Vincken KM et al (2008) Magnetic resonance imaging for quantitative flow measurements in infants with hydrocephalus: a prospective study. J Neurosurg Pediatrics 2:163–170

    Article  Google Scholar 

  102. Lev S, Bhadelia RA, Estin D et al (1997) Functional analysis of third ventricular patency with phase-contrast MRI velocity measurements. Neuroradiology 39:175–179

    Article  CAS  PubMed  Google Scholar 

  103. Linninger AA, Tsakiris C, Zhu DC et al (2005) Pulsatile cerebrospinal fluid dynamics in the human brain. IEEE Trans Biomed Eng 52(4):557–565

    Article  PubMed  Google Scholar 

  104. Longatti P, Basaldella L, Orvieto E et al (2006) Aquaporin(s) expression in choroid plexus tumours. Pediatr Neurosurg 42:228–233

    Article  PubMed  Google Scholar 

  105. Luciano MG, Skarupa DJ, Booth AM et al (2001) Cerebrovascular adaptation in chronic hydrocephalus. J Cereb Blood Flow Metabol 21:285–294

    Article  CAS  Google Scholar 

  106. Lüdemann W, Berens von Rautenfeld D, Samii M, Brinker T (2005) Ultrastructure of the cerebrospinal fluid outflow along the optic nerve into the lymphatic system. Childs Nerv Syst 21:96–103

    Article  PubMed  Google Scholar 

  107. Lüders E, Steinmetz H, Jäcke L (2002) Brain size and grey matter volume in the healthy human brain. NeuroReport 13:2371–2374

    Article  PubMed  Google Scholar 

  108. MacAulay N, Zeuthen T (2010) Water transport between CNS compartments: contributions of aquaporins and co-transporters. Neuroscience 168:941–956

    Article  CAS  PubMed  Google Scholar 

  109. Mack J, Squier W, Eastman JT (2009) Anatomy and development of the meninges. Implications subdural collections and CSF circulation. Pediatr Radiol 39:200–210

    Article  PubMed  Google Scholar 

  110. McAllister JP (2012) Pathophysiology of congenital and neonatal hydrocephalus. Semin Fet Neonat Med 17:285–294

    Article  Google Scholar 

  111. McLone DG (1980) The subarachnoid space: a review. Childs Brain 6:113–130

    CAS  PubMed  Google Scholar 

  112. McLone DG, Knepper PA (1989) The cause of Chiari II malformation: a unified theory. Pediatr Neurosci 15:1–12

    Article  CAS  PubMed  Google Scholar 

  113. Marin-Padilla M (1970) Prenatal and early postnatal ontogenesis of the human motor cortex: a Golgi study. I. The sequential development of the cortical layers. Brain Res 23:167–183

    Article  CAS  PubMed  Google Scholar 

  114. Marin-Padilla M (2012) The human brain intracerebral microvascular system: development and structure. Front Neuroanat 6:38

    Article  PubMed Central  PubMed  Google Scholar 

  115. Matson DD, Crofton FDL (1960) Papilloma of the choroid plexus in childhood. J Neurosurg 17:1002–1027

    Article  CAS  PubMed  Google Scholar 

  116. Miller E, Widjaja E, Blaser S et al (2008) The old and the new: supratentorial MR findings in Chiari II malformations. Childs Nerv Syst 24:563–575

    Article  PubMed  Google Scholar 

  117. Muňoz A, Hinojosa J, Esparza J (2007) Cisternography and ventriculography gadopentetate dimeglumine-enhanced MR imaging in pediatric patients: preliminary report. AJNR Am J Neuroradiol 28:889–894

    PubMed  Google Scholar 

  118. Muszinski C (2010) Posthemorrhagic hydrocephalus. In: Mallucci C, Sgouros S (eds) Cerebrospinal fluid disorders. Informa Healthcare, New York, pp 141–153

    Google Scholar 

  119. Norman MG, O’Kusky JR (1986) The growth and development of the microvasculature in the human cortex. J Neuropathol Exp Neurol 45:222–232

    Article  CAS  PubMed  Google Scholar 

  120. O’Connell JEA (1943) The vascular factor in intracranial pressure and the maintenance of the cerebrospinal fluid circulation. Brain 66:204–228

    Article  Google Scholar 

  121. Ohara S, Nagai H, Matsumoto T, Banno T (1988) MR imaging of CSF pulsatory flow and its relation to intracranial pressure. J Neurosurg 69:675–682

    Article  CAS  PubMed  Google Scholar 

  122. Orešković D, Klarica M, Vukic M (2001) Does the secretion and circulation of the cerebrospinal fluid really exist? Medical Hypothese 56:622–624

    Article  Google Scholar 

  123. OreškovićD KM (2010) The formation of cerebrospinal fluid: nearly a hundred years of interpretations and misinterpretations. Brain Res Rev 64:241–262

    Article  Google Scholar 

  124. Osaka K, Handa H, Matsumoto S, Yasuda M (1980) Development of the cerebrospinal fluid pathway in the normal and abnormal human embryos. Childs Brain 6:26–38

    CAS  PubMed  Google Scholar 

  125. Papadopoulos MC, Verkman AS (2013) Aquaporin water channels in the nervous system. Nat Rev Neurosci 14:265–277

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  126. Papaiconomou C, Zakharov A, Azizi N et al (2004) Reassessment of the pathways responsible for cerebrospinal fluid absorption in the neonate. Childs Nerv Syst 20:29–36

    Article  CAS  PubMed  Google Scholar 

  127. Park EH, Eide PK, Zurakowski D, Madsen JR (2012) Impaired pulsation absorber mechanism in idiopathic normal pressure hydrocephalus. J Neurosurg 117:1189–1196

    Article  PubMed  Google Scholar 

  128. Pasquier L, Marcorelles P, Loget P et al (2009) Rhombencephalosynapsis and related anomalies: a neuropathological study of 40 fetal cases. Acta Neuropathol 117:185–200

    Article  PubMed  Google Scholar 

  129. Passi GR, Bhatnagar S (2015) Rhombencephalosynapsis. Pediatr Neurol 52:551–652

    Article  Google Scholar 

  130. Pellicer A, Valverde E, Gayá F et al (2001) Postnatal adaptation of brain circulation in preterm infants. Pediatr Neurol 24:103–109

    Article  CAS  PubMed  Google Scholar 

  131. Penn RD, Basati S, Sweetman B et al (2011) Ventricle wall movements and cerebrospinal fluid flow in hydrocephalus. J Neurosurg 115:159–164

    Article  PubMed  Google Scholar 

  132. Pennybacker J, Russel DS (1943) Spontaneous ventricular rupture in hydrocephalus with subtentorial cyst formation. J Neurol Psychiatry 6:38–45

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  133. Pettorossi VE, Di Rocco C, Mancinelli et al (1978) Communicating hydrocephalus induced by mechanically increased amplitude of the intraventricular cerebrospinal fluid pulse pressure: rationale and method. Exp Neurol 59:30–39

    Article  CAS  PubMed  Google Scholar 

  134. Pettorossi VE, Di Rocco C, Caldarelli M et al (1978) Influences of phasic changes in systemic blood pressure on intracranial pressure. Eur Neurol 17:216–225

    Article  CAS  PubMed  Google Scholar 

  135. Pollay M (2010) The function and structure of the cerebrospinal fluid outflow system. Cerebrospinal Fluid Res 7:9

    Article  PubMed Central  PubMed  Google Scholar 

  136. 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 191:337–346

    Article  PubMed Central  PubMed  Google Scholar 

  137. Purin VR (1963) The importance of the cerebrospinal fluid system to the developing brain. In: Klosovskii BN (ed) The development of the brain and its disturbance by harmful factors. Pergamon, London, pp 83–95

    Google Scholar 

  138. Rash JE, Yasamura T, Hudson CS et al (1998) Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc Natl Acad Sci U S A 95:11981–11986

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  139. Raybaud C, Ahmad T, Rastegar et al (2013) The premature brain: developmental and lesional anatomy. Neuroradiology 55(Suppl 2):S23–S40

    Article  Google Scholar 

  140. Redzic ZB, Preston JE, Duncan JA et al (2005) The choroid plexus-cerebrospinal fluid system: from development to aging. Cur Top Develop Biol 71:1–52

    Article  CAS  Google Scholar 

  141. Rekate HL, Erwood S, Brodkey JA et al. (1985–1986) Etiology of ventriculomegaly in choroid plexus papilloma. Pediatr Neurosci 12:196–201

  142. Rekate HL, Nadkarni TD, Wallace D (2008) The importance of the cortical subarachnoid space in understanding hydrocephalus. J Neurosurg Pediatrics 2:1–11

    Article  Google Scholar 

  143. Rekate HL (2011) A consensus on the classification of hydrocephalus: its utility in the assessment of abnormalities of cerebrospinal fluid dynamics. Childs Nerv Syst 27:1535–1541

    Article  PubMed Central  PubMed  Google Scholar 

  144. Rennels ML, Gregory TF, Blaumanis OB et al (1985) Evidence for a “paravascular” fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res 326:47–63

    Article  CAS  PubMed  Google Scholar 

  145. Rhoton AL (2000) The posterior fossa cisterns. Neurosurgery 47(3 Suppl):S287–S297

    Article  PubMed  Google Scholar 

  146. Roales-Buján R, Páez P, Guerra M et al (2012) Astrocytes acquire morphological and functional characteristics of ependymal cells following disruption of ependyma in hydrocephalus. Acta Neuropathol 124:531–546

    Article  PubMed Central  PubMed  Google Scholar 

  147. Robinson S (2012) Neonatal post hemorrhagic hydrocephalus from prematurity: pathophysiology and current treatment concepts. A review J Neurosurg Pediatrics 9:242–258

    Article  Google Scholar 

  148. Rodriguez EM, Guerra MM, Vio K et al (2012) A cell junction pathology of neural stem cells leads to abnormal neurogenesis and hydrocephalus. Biol Res 45:231–241

    Article  PubMed  CAS  Google Scholar 

  149. Shirane R, Sato S, Sato K et al (1992) Cerebral blood flow and oxygen metabolism in infants with hydrocephalus. Childs Nerv Syst 8:118–123

    Article  CAS  PubMed  Google Scholar 

  150. Sival DA, Guerra M, den Dunnen WFA et al (2011) Neuroependymal denudation is in progress in full-term human foetal spina bifida aperta. Brain Pathol 21:163–179

    Article  CAS  PubMed  Google Scholar 

  151. Siyahhan B, Knobloch V, de Zélicourt D et al (2014) Flow induced by ependymal cilia dominates near-wall cerebrospinal fluid dynamics in the lateral ventricles. J R Soc Interface 11:20131189

    Article  PubMed Central  PubMed  Google Scholar 

  152. Spector R, Keep RF, Snodgrass SR et al (2015) A balanced view of choroid plexus structure and function: focus on adult humans. Exp Neurol 267:78–86

    Article  PubMed  Google Scholar 

  153. Staudt M, Braun C, Gerloff C et al (2006) Developing somatosensory projections bypass periventricular brain lesions. Neurology 67:522–525

    Article  CAS  PubMed  Google Scholar 

  154. Staudt M (2010) Reorganization after pre- and perinatal brain lesions. J Anat 217:469–474

    Article  PubMed Central  PubMed  Google Scholar 

  155. Stephensen H, Tisell M, Wikkelsö C (2002) There is no transmantle pressure gradient in communicating or noncommunicating hydrocephalus. Neurosurgery 50:763–773

    Article  PubMed  Google Scholar 

  156. Strik C, Klose U, Erb M et al (2002) Intracranial oscillations of cerebrospinal fluid and blood flow: analysis with magnetic resonance imaging. J Magn Res Imag 15:251–258

    Article  Google Scholar 

  157. Stroobandt G, Thauvoy C, Gilliard C et al (1988) Papilloma of the choroid plexus of the lateral ventricle without generalized hydrocephalus. Neurochirurgie 34:128–132, in French

    CAS  PubMed  Google Scholar 

  158. Tripathi BJ, Tripathi RC (1974) Vacuolar transcellular channels as a drainage pathway for cerebrospinal fluid. J Physiol 239:195–206

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  159. Tsitouras V, Sgouros S (2011) Infantile posthemorrhagic hydrocephalus. Childs Nerv Syst 27:1595–1608

    Article  PubMed  Google Scholar 

  160. Vanneste J, Augustijn P, Davies GA et al (1992) Normal pressure hydrocephalus: is cisternography still useful in selecting patients for a shunt? Arch Neurol 49:366–370

    Article  CAS  PubMed  Google Scholar 

  161. Virhammar J, Laurell K, Ahlgren A et al (2014) Idiopathic normal pressure hydrocephalus: cerebral perfusion measured with pCASL before and repeatedly after CSF removal. J Cereb Blood Flow Metab 34:1771–1778

    Article  PubMed Central  PubMed  Google Scholar 

  162. Volpe JJ (2001) Neurology of the newborn, 4th edn. Saunders, Philadelphia

    Google Scholar 

  163. Wagner C, Batiz LF, Rodriguez S et al (2003) Cellular mechanisms involved in the stenosis and obliteration of the cerebral aqueduct of hyh mutant mice developing congenital hydrocephalus. J Neuropathol Exp Neurol 62:1019–1040

    Article  CAS  PubMed  Google Scholar 

  164. Wagshul ME, Chen JJ, Egnor MR et al (2006) Amplitude and phase of cerebrospinal fluid pulsations: experimental studies and review of the literature. J Neurosurg 104:810–819

    Article  PubMed  Google Scholar 

  165. Wagshul ME, Eide PK, Madsen JR (2011) The pulsating brain: a review of experimental and clinical studies of intracranial pulsatility. Fluids Barriers CNS 8:5

    Article  PubMed Central  PubMed  Google Scholar 

  166. Wake H, Lee PR, Fields RD (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333:1647–1651

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  167. Worthington WC, Cathcart RS (1966) Ciliary currents on ependymal surfaces. Ann NY Acad Sci 130:944–950

    Article  PubMed  Google Scholar 

  168. Wünschmann A, Oglesbee M (2001) Periventricular changes associated with spontaneous canine hydrocephalus. Vet Pathol 38:67–73

    Article  PubMed  Google Scholar 

  169. Xenos C, Sgouros S, Natarajan K (2002) Ventricular volume change in childhood. J Neurosurg 97:584–590

    Article  PubMed  Google Scholar 

  170. Yamada S, Miyazaki M, Kanazawa H et al (2008) Visualization of the cerebrospinal fluid movement with spin labeling at MR imaging. Preliminary results in normal and pathophysiologic conditions. Radiology 249(2):644–652

    Article  PubMed  Google Scholar 

  171. Yamasaki M, Thompson P, Lemmon V (1997) CRASH syndrome: mutations in L1CAM correlate with severity of the disease. Neuropediatrics 28:175–178

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  172. Yamasaki M, Nonaka M, Bamba Y et al (2012) Diagnosis, treatment and long-term outcomes of fetal hydrocephalus. Semin Fet Neonat Med 17:330–335

    Article  Google Scholar 

  173. Yasuda T, Tomita T, McLone DG, Donovan M (2002) Measurements of cerebrospinal fluid output through external ventricular drainage in one hundred infants and children: correlation with cerebrospinal fluid production. Pediatr Neurosurg 36:22–28

    Article  PubMed  Google Scholar 

  174. Yeom KW, Lober RM, Alexander A et al (2014) Hydrocephalus decreases arterial spin-labeled cerebral perfusion. AJNR Am J Neuroradiol 35:1433–1439

    Article  CAS  PubMed  Google Scholar 

  175. Zahl SM, Egge A, Helseth E, Wester K (2011) Benign external hydrocephalus: a review, with emphasis on management. Neurosurg Rev 34:417–432

    Article  PubMed Central  PubMed  Google Scholar 

  176. Zhang ET, Inman CBE, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:111–123

    CAS  PubMed Central  PubMed  Google Scholar 

  177. Zhu XL, Di Rocco C (2013) Choroid plexus coagulation for hydrocephalus not due to CSF overproduction: a review. Childs Nerv Syst 29:35–42

    Article  PubMed  Google Scholar 

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    Charles Raybaud

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Raybaud, C. MR assessment of pediatric hydrocephalus: a road map. Childs Nerv Syst 32, 19–41 (2016). https://doi.org/10.1007/s00381-015-2888-y

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