Anatomy and Physiology-Based Magnetic Resonance Imaging in Hydrocephalus

  • Smruti K. Patel
  • Shawn M. Vuong
  • Weihong Yuan
  • Francesco T. ManganoEmail author


The development of advanced neuroimaging techniques over the past several decades has served a critical role in the diagnosis and treatment of hydrocephalus. The latest evidence from both human and animal research suggests that one of the major pathophysiological mechanisms underlying poor outcomes in these patients is damage to vulnerable white matter structures in the brain due to ventricular enlargement and increased intracranial pressure. However, a clear understanding of these white matter abnormalities and their implications on neurobehavioral outcomes in this patient population is not well understood. To this end, magnetic resonance techniques such as diffusion tensor imaging, probabilistic diffusion tractography, and elastography, to name a few, have recently been studied to assess noninvasive quantification of these abnormalities and the biomechanics of brain tissue. Our chapter examines the evolution of magnetic resonance neuroimaging technology in hydrocephalus. We particularly focus on the use of anatomy and physiology-based imaging techniques and diffusion tensor imaging which are supported by a growing body of literature as promising noninvasive tools in the diagnosis and long-term management. We conclude with a brief discussion on more novel, emerging techniques such as magnetic resonance elastography and experimental imaging such as synthetic magnetic resonance imaging.


pediatric hydrocephalus benign external hydrocephalus normal pressure hydrocephalus magnetic resonance imaging phase contrast MRI 3D-CISS diffusion tensor imaging fractional anisotropy white matter injury MR elastography synthetic MRI 


  1. 1.
    Simon TD, Riva-Cambrin J, Srivastava R, Bratton SL, Dean JM, Kestle JR, et al. Hospital care for children with hydrocephalus in the United States: utilization, charges, comorbidities, and deaths. J Neurosurg Pediatr. 2008;1(2):131–7.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Siasios I, Kapsalaki EZ, Fountas KN, Fotiadou A, Dorsch A, Vakharia K, et al. The role of diffusion tensor imaging and fractional anisotropy in the evaluation of patients with idiopathic normal pressure hydrocephalus: a literature review. Neurosurg Focus. 2016;41(3):E12.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Del Bigio MR. Neuropathology and structural changes in hydrocephalus. Dev Disabil Res Rev. 2010;16(1):16–22.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Del Bigio MR. Cellular damage and prevention in childhood hydrocephalus. Brain Pathol. 2004;14(3):317–24.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Del Bigio MR. Pathophysiologic consequences of hydrocephalus. Neurosurg Clin N Am. 2001;12(4):639–49, vii.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Del Bigio MR, da Silva MC, Drake JM, Tuor UI. Acute and chronic cerebral white matter damage in neonatal hydrocephalus. Can J Neurol Sci. 1994;21(4):299–305.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Khan OH, Enno TL, Del Bigio MR. Brain damage in neonatal rats following kaolin induction of hydrocephalus. Exp Neurol. 2006;200(2):311–20.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Del Bigio MR, Zhang YW. Cell death, axonal damage, and cell birth in the immature rat brain following induction of hydrocephalus. Exp Neurol. 1998;154(1):157–69.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    McAllister JP. Getting to the root of hydrocephalus. Sci Transl Med. 2011;3(99):99fs4.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Kahle KT, Kulkarni AV, Limbrick DD Jr, Warf BC. Hydrocephalus in children. Lancet. 2016;387(10020):788–99.CrossRefGoogle Scholar
  11. 11.
    Drake JM. The surgical management of pediatric hydrocephalus. Neurosurgery. 2008;62(Suppl 2):633–40; discussion 40–2.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Koral K, Blackburn T, Bailey AA, Koral KM, Anderson J. Strengthening the argument for rapid brain MR imaging: estimation of reduction in lifetime attributable risk of developing fatal cancer in children with shunted hydrocephalus by instituting a rapid brain MR imaging protocol in lieu of Head CT. AJNR Am J Neuroradiol. 2012;33(10):1851–4.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Patel DM, Tubbs RS, Pate G, Johnston JM Jr, Blount JP. Fast-sequence MRI studies for surveillance imaging in pediatric hydrocephalus. J Neurosurg Pediatr. 2014;13(4):440–7.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Patel MR, Klufas RA, Alberico RA, Edelman RR. Half-fourier acquisition single-shot turbo spin-echo (HASTE) MR: comparison with fast spin-echo MR in diseases of the brain. AJNR Am J Neuroradiol. 1997;18(9):1635–40.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Dincer A, Ozek MM. Radiologic evaluation of pediatric hydrocephalus. Childs Nerv Syst. 2011;27(10):1543–62.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Battal B, Kocaoglu M, Bulakbasi N, Husmen G, Tuba Sanal H, Tayfun C. Cerebrospinal fluid flow imaging by using phase-contrast MR technique. Br J Radiol. 2011;84(1004):758–65.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Yamada S, Tsuchiya K, Bradley WG, Law M, Winkler ML, Borzage MT, et al. Current and emerging MR imaging techniques for the diagnosis and management of CSF flow disorders: a review of phase-contrast and time-spatial labeling inversion pulse. AJNR Am J Neuroradiol. 2015;36(4):623–30.CrossRefGoogle Scholar
  18. 18.
    Greitz D. Paradigm shift in hydrocephalus research in legacy of Dandy’s pioneering work: rationale for third ventriculostomy in communicating hydrocephalus. Childs Nerv Syst. 2007;23(5):487–9.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Greitz D. The hydrodynamic hypothesis versus the bulk flow hypothesis. Neurosurg Rev. 2004;27(4):299–300.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Wagshul ME, Chen JJ, Egnor MR, McCormack EJ, Roche PE. Amplitude and phase of cerebrospinal fluid pulsations: experimental studies and review of the literature. J Neurosurg. 2006;104(5):810–9.CrossRefGoogle Scholar
  21. 21.
    Greitz D. Radiological assessment of hydrocephalus: new theories and implications for therapy. Neurosurg Rev. 2004;27(3):145–65; discussion 66–7.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Wagshul ME, Eide PK, Madsen JR. The pulsating brain: a review of experimental and clinical studies of intracranial pulsatility. Fluids Barriers CNS. 2011;8(1):5.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Stivaros SM, Sinclair D, Bromiley PA, Kim J, Thorne J, Jackson A. Endoscopic third ventriculostomy: predicting outcome with phase-contrast MR imaging. Radiology. 2009;252(3):825–32.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Bargallo N, Olondo L, Garcia AI, Capurro S, Caral L, Rumia J. Functional analysis of third ventriculostomy patency by quantification of CSF stroke volume by using cine phase-contrast MR imaging. AJNR Am J Neuroradiol. 2005;26(10):2514–21.PubMedPubMedCentralGoogle Scholar
  25. 25.
    McCormack EJ, Egnor MR, Wagshul ME. Improved cerebrospinal fluid flow measurements using phase contrast balanced steady-state free precession. Magn Reson Imaging. 2007;25(2):172–82.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Brandner S, Buchfelder M, Eyuepoglu IY, Luecking H, Doerfler A, Stadlbauer A. Visualization of CSF flow with time-resolved 3D MR velocity mapping in aqueductal stenosis before and after endoscopic third ventriculostomy: a feasibility study. Clin Neuroradiol. 2018;28(1):69–74.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Algin O. Prediction of endoscopic third ventriculostomy (ETV) success with 3D-SPACE technique. Neurosurg Rev. 2015;38(2):395–7.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Algin O, Ucar M, Ozmen E, Borcek AO, Ozisik P, Ocakoglu G, et al. Assessment of third ventriculostomy patency with the 3D-SPACE technique: a preliminary multicenter research study. J Neurosurg. 2015;122(6):1347–55.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Yamada S, Miyazaki M, Kanazawa H, Higashi M, Morohoshi Y, Bluml S, et al. Visualization of cerebrospinal fluid movement with spin labeling at MR imaging: preliminary results in normal and pathophysiologic conditions. Radiology. 2008;249(2):644–52.CrossRefGoogle Scholar
  30. 30.
    Gandhoke GS, Frassanito P, Chandra N, Ojha BK, Singh A. Role of magnetic resonance ventriculography in multiloculated hydrocephalus. J Neurosurg Pediatr. 2013;11(6):697–703.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Joseph VB, Raghuram L, Korah IP, Chacko AG. MR ventriculography for the study of CSF flow. AJNR Am J Neuroradiol. 2003;24(3):373–81.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Singh I, Haris M, Husain M, Husain N, Rastogi M, Gupta RK. Role of endoscopic third ventriculostomy in patients with communicating hydrocephalus: an evaluation by MR ventriculography. Neurosurg Rev. 2008;31(3):319–25.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Del Bigio MR. Neuropathological changes caused by hydrocephalus. Acta Neuropathol. 1993;85(6):573–85.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Del Bigio MR, Cardoso ER, Halliday WC. Neuropathological changes in chronic adult hydrocephalus: cortical biopsies and autopsy findings. Can J Neurol Sci. 1997;24(2):121–6.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Buckley RT, Yuan W, Mangano FT, Phillips JM, Powell S, McKinstry RC, et al. Longitudinal comparison of diffusion tensor imaging parameters and neuropsychological measures following endoscopic third ventriculostomy for hydrocephalus. J Neurosurg Pediatr. 2012;9(6):630–5.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Mataro M, Junque C, Poca MA, Sahuquillo J. Neuropsychological findings in congenital and acquired childhood hydrocephalus. Neuropsychol Rev. 2001;11(4):169–78.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Kulkarni AV, Donnelly R, Mabbott DJ, Widjaja E. Relationship between ventricular size, white matter injury, and neurocognition in children with stable, treated hydrocephalus. J Neurosurg Pediatr. 2015;16(3):267–74.PubMedCrossRefGoogle Scholar
  38. 38.
    Warf B, Ondoma S, Kulkarni A, Donnelly R, Ampeire M, Akona J, et al. Neurocognitive outcome and ventricular volume in children with myelomeningocele treated for hydrocephalus in Uganda. J Neurosurg Pediatr. 2009;4(6):564–70.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Azab WA, Mijalcic RM, Nakhi SB, Mohammad MH. Ventricular volume and neurocognitive outcome after endoscopic third ventriculostomy: is shunting a better option? A review. Childs Nerv Syst. 2016;32(5):775–80.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Mandell JG, Kulkarni AV, Warf BC, Schiff SJ. Volumetric brain analysis in neurosurgery: Part 2. Brain and CSF volumes discriminate neurocognitive outcomes in hydrocephalus. J Neurosurg Pediatr. 2015;15(2):125–32.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Assaf Y, Ben-Sira L, Constantini S, Chang LC, Beni-Adani L. Diffusion tensor imaging in hydrocephalus: initial experience. AJNR Am J Neuroradiol. 2006;27(8):1717–24.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Yuan W, Mangano FT, Air EL, Holland SK, Jones BV, Altaye M, et al. Anisotropic diffusion properties in infants with hydrocephalus: a diffusion tensor imaging study. AJNR Am J Neuroradiol. 2009;30(9):1792–8.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Yuan W, Deren KE, McAllister JP 2nd, Holland SK, Lindquist DM, Cancelliere A, et al. Diffusion tensor imaging correlates with cytopathology in a rat model of neonatal hydrocephalus. Cerebrospinal Fluid Res. 2010;7:19.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Air EL, Yuan W, Holland SK, Jones BV, Bierbrauer K, Altaye M, et al. Longitudinal comparison of pre- and postoperative diffusion tensor imaging parameters in young children with hydrocephalus. J Neurosurg Pediatr. 2010;5(4):385–91.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Sun M, Yuan W, Hertzler DA, Cancelliere A, Altaye M, Mangano FT. Diffusion tensor imaging findings in young children with benign external hydrocephalus differ from the normal population. Childs Nerv Syst. 2012;28(2):199–208.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Yuan W, McAllister JP 2nd, Lindquist DM, Gill N, Holland SK, Henkel D, et al. Diffusion tensor imaging of white matter injury in a rat model of infantile hydrocephalus. Childs Nerv Syst. 2012;28(1):47–54.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Yuan W, McKinstry RC, Shimony JS, Altaye M, Powell SK, Phillips JM, et al. Diffusion tensor imaging properties and neurobehavioral outcomes in children with hydrocephalus. AJNR Am J Neuroradiol. 2013;34(2):439–45.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Mangano FT, Altaye M, McKinstry RC, Shimony JS, Powell SK, Phillips JM, et al. Diffusion tensor imaging study of pediatric patients with congenital hydrocephalus: 1-year postsurgical outcomes. J Neurosurg Pediatr. 2016;18(3):306–19.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics. 2007;4(3):316–29.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Yuan Y, Zhu H, Styner M, Gilmore JH, Marron JS. Varying coefficient model for modeling diffusion tensors along white matter tracts. Ann Appl Stat. 2013;7(1):102–25.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Rajagopal A, Shimony JS, McKinstry RC, Altaye M, Maloney T, Mangano FT, et al. White matter microstructural abnormality in children with hydrocephalus detected by probabilistic diffusion tractography. AJNR Am J Neuroradiol. 2013;34(12):2379–85.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Cancelliere A, Mangano FT, Air EL, Jones BV, Altaye M, Rajagopal A, et al. DTI values in key white matter tracts from infancy through adolescence. AJNR Am J Neuroradiol. 2013;34(7):1443–9.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Yuan W, McAllister JP, Mangano FT. Neuroimaging of white matter abnormalities in pediatric hydrocephalus. J Pediatr Neuroradiol. 2013;2:119–28.CrossRefGoogle Scholar
  54. 54.
    Ben-Sira L, Goder N, Bassan H, Lifshits S, Assaf Y, Constantini S. Clinical benefits of diffusion tensor imaging in hydrocephalus. J Neurosurg Pediatr. 2015;16(2):195–202.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Hasan KM, Eluvathingal TJ, Kramer LA, Ewing-Cobbs L, Dennis M, Fletcher JM. White matter microstructural abnormalities in children with spina bifida myelomeningocele and hydrocephalus: a diffusion tensor tractography study of the association pathways. J Magn Reson Imaging. 2008;27(4):700–9.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Mukherjee P, Miller JH, Shimony JS, Philip JV, Nehra D, Snyder AZ, et al. Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. AJNR Am J Neuroradiol. 2002;23(9):1445–56.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Yuan W, Holland SK, Shimony JS, Altaye M, Mangano FT, Limbrick DD, et al. Abnormal structural connectivity in the brain networks of children with hydrocephalus. Neuroimage Clin. 2015;8:483–92.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Yuan W, Meller A, Shimony JS, Nash T, Jones BV, Holland SK, et al. Left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgery. Neuroimage Clin. 2016;12:631–9.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH. Symptomatic occult hydrocephalus with “normal” cerebrospinal-fluid pressure. A treatable syndrome. N Engl J Med. 1965;273:117–26.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Hakim S, Adams RD. The special clinical problem of symptomatic hydrocephalus with normal cerebrospinal fluid pressure. Observations on cerebrospinal fluid hydrodynamics. J Neurol Sci. 1965;2(4):307–27.CrossRefGoogle Scholar
  61. 61.
    Keong NC, Price SJ, Gillard JH, Pickard JD. DTI profiles in NPH. Br J Neurosurg. 2012;26(5):600.Google Scholar
  62. 62.
    Keong NC, Pena A, Price SJ, Czosnyka M, Czosnyka Z, DeVito EE, et al. Diffusion tensor imaging profiles reveal specific neural tract distortion in normal pressure hydrocephalus. PLoS One. 2017;12(8):e0181624.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Hattingen E, Jurcoane A, Melber J, Blasel S, Zanella FE, Neumann-Haefelin T, et al. Diffusion tensor imaging in patients with adult chronic idiopathic hydrocephalus. Neurosurgery. 2010;66(5):917–24.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Ivkovic M, Liu B, Ahmed F, Moore D, Huang C, Raj A, et al. Differential diagnosis of normal pressure hydrocephalus by MRI mean diffusivity histogram analysis. AJNR Am J Neuroradiol. 2013;34(6):1168–74.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Hattori T, Yuasa T, Aoki S, Sato R, Sawaura H, Mori T, et al. Altered microstructure in corticospinal tract in idiopathic normal pressure hydrocephalus: comparison with Alzheimer disease and Parkinson disease with dementia. AJNR Am J Neuroradiol. 2011;32(9):1681–7.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Hong YJ, Yoon B, Shim YS, Cho AH, Lim SC, Ahn KJ, et al. Differences in microstructural alterations of the hippocampus in Alzheimer disease and idiopathic normal pressure hydrocephalus: a diffusion tensor imaging study. AJNR Am J Neuroradiol. 2010;31(10):1867–72.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Kim MJ, Seo SW, Lee KM, Kim ST, Lee JI, Nam DH, et al. Differential diagnosis of idiopathic normal pressure hydrocephalus from other dementias using diffusion tensor imaging. AJNR Am J Neuroradiol. 2011;32(8):1496–503.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Girard NJ, Raybaud CA. Ventriculomegaly and pericerebral CSF collection in the fetus: early stage of benign external hydrocephalus? Childs Nerv Syst. 2001;17(4–5):239–45.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Smith R, Leonidas JC, Maytal J. The value of head ultrasound in infants with macrocephaly. Pediatr Radiol. 1998;28(3):143–6.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Kumar R. External hydrocephalus in small children. Childs Nerv Syst. 2006;22(10):1237–41.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Scheel M, Diekhoff T, Sprung C, Hoffmann KT. Diffusion tensor imaging in hydrocephalus–findings before and after shunt surgery. Acta Neurochir. 2012;154(9):1699–706.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Patel SK, Yuan W, Mangano FT. Advanced Neuroimaging Techniques in Pediatric Hydrocephalus. Pediatr Neurosurg. 2017;52:436.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Yuan W, Harpster K, Jones BV, Shimony JS, McKinstry RC, Weckherlin N, et al. Changes of white matter diffusion anisotropy in response to a 6-week iPad application-based occupational therapy intervention in children with surgically treated hydrocephalus: a pilot study. Neuropediatrics. 2016;47(5):336–40.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Hatta J, Hatta T, Moritake K, Otani H. Heavy water inhibiting the expression of transforming growth factor-beta1 and the development of kaolin-induced hydrocephalus in mice. J Neurosurg. 2006;104(4 Suppl):251–8.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Slobodian I, Krassioukov-Enns D, Del Bigio MR. Protein and synthetic polymer injection for induction of obstructive hydrocephalus in rats. Cerebrospinal Fluid Res. 2007;4:9.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Cohen AR, Leifer DW, Zechel M, Flaningan DP, Lewin JS, Lust WD. Characterization of a model of hydrocephalus in transgenic mice. J Neurosurg. 1999;91(6):978–88.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Emmert AS, Goto J, Shula C, Qin S, Hu Y, Mangano FT, editors. CRISPR/cas9-based development of novel transgenic rat model of x-linked hydrocephalus. Joint Congress of the International Children’s Continence Society (ICCS) and The Society For Research Into Hydroephalus And Spina Bifida (SRHSB); 2017; St. Louis, MO.Google Scholar
  78. 78.
    Emmert A, Vuong S, Shula C, Hu Y, Goto J, Mangano FT, editors. CRISPR/Cas9-based development of novel transgenic rat model of X-linked hydrocephalus: diffusion tensor imaging provides mild white abnormalities in a CRISPR/Cas9-Generated [Abstract]. 46th Annual AANS/CNS Section on Pediatric Neurological Surgery Meeting; 2017; Houston, TX.Google Scholar
  79. 79.
    Eskandari R, Abdullah O, Mason C, Lloyd KE, Oeschle AN, McAllister JP 2nd. Differential vulnerability of white matter structures to experimental infantile hydrocephalus detected by diffusion tensor imaging. Childs Nerv Syst. 2014;30(10):1651–61.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Aojula A, Botfield H, McAllister JP 2nd, Gonzalez AM, Abdullah O, Logan A, et al. Diffusion tensor imaging with direct cytopathological validation: characterisation of decorin treatment in experimental juvenile communicating hydrocephalus. Fluids Barriers CNS. 2016;13(1):9.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Betts AM, Leach JL, Jones BV, Zhang B, Serai S. Brain imaging with synthetic MR in children: clinical quality assessment. Neuroradiology. 2016;58:1017.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Blystad I, Warntjes JB, Smedby O, Landtblom AM, Lundberg P, Larsson EM. Synthetic MRI of the brain in a clinical setting. Acta Radiol. 2012;53(10):1158–63.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Ambarki K, Lindqvist T, Wahlin A, Petterson E, Warntjes MJ, Birgander R, et al. Evaluation of automatic measurement of the intracranial volume based on quantitative MR imaging. AJNR Am J Neuroradiol. 2012;33(10):1951–6.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Virhammar J, Warntjes M, Laurell K, Larsson EM. Quantitative MRI for rapid and user-independent monitoring of intracranial CSF volume in hydrocephalus. AJNR Am J Neuroradiol. 2016;37(5):797–801.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Hagiwara A, Warntjes M, Hori M, Andica C, Nakazawa M, Kumamaru KK, et al. SyMRI of the brain: rapid quantification of relaxation rates and proton density, with synthetic MRI, automatic brain segmentation, and myelin measurement. Investig Radiol. 2017;52(10):647–57.CrossRefGoogle Scholar
  86. 86.
    Fattahi N, Arani A, Perry A, Meyer F, Manduca A, Glaser K, et al. MR elastography demonstrates increased brain stiffness in normal pressure hydrocephalus. AJNR Am J Neuroradiol. 2016;37(3):462–7.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Hirsch S, Beyer F, Guo J, Papazoglou S, Tzschaetzsch H, Braun J, et al. Compression-sensitive magnetic resonance elastography. Phys Med Biol. 2013;58(15):5287–99.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Mousavi SR, Fehlner A, Streitberger KJ, Braun J, Samani A, Sack I. Measurement of in vivo cerebral volumetric strain induced by the Valsalva maneuver. J Biomech. 2014;47(7):1652–7.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Pong AC, Juge L, Bilston LE, Cheng S. Development of acute hydrocephalus does not change brain tissue mechanical properties in adult rats, but in juvenile rats. PLoS One. 2017;12(8):e0182808.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Juge L, Pong AC, Bongers A, Sinkus R, Bilston LE, Cheng S. Changes in rat brain tissue microstructure and stiffness during the development of experimental obstructive hydrocephalus. PLoS One. 2016;11(2):e0148652.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Smruti K. Patel
    • 1
  • Shawn M. Vuong
    • 1
  • Weihong Yuan
    • 2
  • Francesco T. Mangano
    • 1
    Email author
  1. 1.Division of Pediatric Neurosurgery, Cincinnati Children’s Hospital Medical Center, Department of Neurological SurgeryUniversity of Cincinnati College of MedicineCincinnatiUSA
  2. 2.Department of RadiologyUniversity of Cincinnati, Cincinnati Children’s Hospital Medical CenterCincinnatiUSA

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