Skip to main content
Top
Published in: European Radiology 11/2018

01-11-2018 | Magnetic Resonance

Changes in sensorimotor-related thalamic diffusion properties and cerebrospinal fluid hydrodynamics predict gait responses to tap test in idiopathic normal-pressure hydrocephalus

Authors: Ping-Huei Tsai, Yung-Chieh Chen, Shih-Wei Chiang, Teng-Yi Huang, Ming-Chung Chou, Hua-Shan Liu, Hsiao-Wen Chung, Giia-Sheun Peng, Hsin-I Ma, Hung-Wen Kao, Cheng-Yu Chen

Published in: European Radiology | Issue 11/2018

Login to get access

Abstract

Objectives

To compare diffusion tensor (DT)-derived indices from the thalamic nuclei and cerebrospinal fluid (CSF) hydrodynamic parameters for the prediction of gait responsiveness to the CSF tap test in early iNPH patients.

Methods

In this study, 22 patients with iNPH and 16 normal controls were enrolled with the approval of an institutional review board. DT imaging and phase-contrast magnetic resonance imaging were performed in patients and controls to determine DT-related indices of the sensorimotor-related thalamic nuclei and CSF hydrodynamics. Gait performance was assessed in patients using gait scale before and after the tap test. The Mann-Whitney U test and receiver operating characteristic (ROC) curve analysis were applied to compare group differences between patients and controls and assess the predictive performance of gait responsiveness to the tap test in the patients.

Results

Fractional anisotropy (FA) and axial diffusivity showed significant increases in the ventrolateral (VL) and ventroposterolateral (VPL) nuclei of the iNPH group compared with those of the control group (p < 0.05). The predictions of gait responsiveness of ventral thalamic FA alone (area under the ROC curve [AUC] < 0.8) significantly outperformed those of CSF hydrodynamics alone (AUC < 0.6). The AUC curve was elevated to 0.812 when the CSF peak systolic velocity and FA value were combined for the VPL nucleus, yielding the highest sensitivity (0.769) and specificity (0.778) to predict gait responses.

Conclusions

Combined measurements of sensorimotor-related thalamic FA and CSF hydrodynamics can provide potential biomarkers for gait response to the CSF tap test in patients with iNPH.

Key Points

Ventrolateral and ventroposterolateral thalamic FA may predict gait responsiveness to tap test.
Thalamic neuroplasticity can be assessed through DTI in idiopathic normal-pressure hydrocephalus.
Changes in the CST associated with gait control could trigger thalamic neuroplasticity.
Activities of sensorimotor-related circuits could alter in patients with gait disturbance.
Management of patients with iNPH could be more appropriate.
Appendix
Available only for authorised users
Literature
1.
go back to reference Andrén K, Wikkelsø C, Tisell M, Hellström P (2014) Natural course of idiopathic normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry 85:806–810CrossRef Andrén K, Wikkelsø C, Tisell M, Hellström P (2014) Natural course of idiopathic normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry 85:806–810CrossRef
2.
go back to reference Williams MA, Relkin NR (2013) Diagnosis and management of idiopathic normal-pressure hydrocephalus. Neurol Clin Pract 3:375–385CrossRef Williams MA, Relkin NR (2013) Diagnosis and management of idiopathic normal-pressure hydrocephalus. Neurol Clin Pract 3:375–385CrossRef
3.
go back to reference Hakim S, Adams RD (1965) The special clinical problem of symptomatic hydrocephalus with normal cerebrospinal fluid pressure. Observations on cerebrospinal fluid hydrodynamics. J Neurol Sci 2:307–327CrossRef Hakim S, Adams RD (1965) The special clinical problem of symptomatic hydrocephalus with normal cerebrospinal fluid pressure. Observations on cerebrospinal fluid hydrodynamics. J Neurol Sci 2:307–327CrossRef
4.
go back to reference Scollato A, Tenenbaum R, Bahl G, Celerini M, Salani B, Di Lorenzo N (2008) Changes in aqueductal CSF stroke volume and progression of symptoms in patients with unshunted idiopathic normal pressure hydrocephalus. AJNR Am J Neuroradiol 29:192–197CrossRef Scollato A, Tenenbaum R, Bahl G, Celerini M, Salani B, Di Lorenzo N (2008) Changes in aqueductal CSF stroke volume and progression of symptoms in patients with unshunted idiopathic normal pressure hydrocephalus. AJNR Am J Neuroradiol 29:192–197CrossRef
5.
go back to reference Ravdin LD, Katzen HL, Jackson AE, Tsakanikas D, Assuras S, Relkin NR (2008) Features of gait most responsive to tap test in normal pressure hydrocephalus. Clin Neurol Neurosurg 110:455–461CrossRef Ravdin LD, Katzen HL, Jackson AE, Tsakanikas D, Assuras S, Relkin NR (2008) Features of gait most responsive to tap test in normal pressure hydrocephalus. Clin Neurol Neurosurg 110:455–461CrossRef
6.
go back to reference Chen IH, Huang CI, Liu HC, Chen KK (1994) Effectiveness of shunting in patients with normal pressure hydrocephalus predicted by temporary, controlled-resistance, continuous lumbar drainage: a pilot study. J Neurol Neurosurg Psychiatry 57:1430–1432CrossRef Chen IH, Huang CI, Liu HC, Chen KK (1994) Effectiveness of shunting in patients with normal pressure hydrocephalus predicted by temporary, controlled-resistance, continuous lumbar drainage: a pilot study. J Neurol Neurosurg Psychiatry 57:1430–1432CrossRef
7.
go back to reference Virhammar J, Cesarini KG, Laurell K (2012) The CSF tap test in normal pressure hydrocephalus: evaluation time, reliability and the influence of pain. Eur J Neurol 19:271–276CrossRef Virhammar J, Cesarini KG, Laurell K (2012) The CSF tap test in normal pressure hydrocephalus: evaluation time, reliability and the influence of pain. Eur J Neurol 19:271–276CrossRef
8.
go back to reference Yamada S, Tsuchiya K, Bradley WG et al (2015) 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 36:623–630CrossRef Yamada S, Tsuchiya K, Bradley WG et al (2015) 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 36:623–630CrossRef
9.
go back to reference Dixon GR, Friedman JA, Luetmer PH et al (2002) Use of cerebrospinal fluid flow rates measured by phase-contrast MR to predict outcome of ventriculoperitoneal shunting for idiopathic normal-pressure hydrocephalus. Mayo Clin Proc 77:509–514CrossRef Dixon GR, Friedman JA, Luetmer PH et al (2002) Use of cerebrospinal fluid flow rates measured by phase-contrast MR to predict outcome of ventriculoperitoneal shunting for idiopathic normal-pressure hydrocephalus. Mayo Clin Proc 77:509–514CrossRef
10.
go back to reference Mase M, Yamada K, Banno T, Miyachi T, Ohara S, Matsumoto T (1998) Quantitative analysis of CSF flow dynamics using MRI in normal pressure hydrocephalus. Acta Neurochir Suppl 71:350–353PubMed Mase M, Yamada K, Banno T, Miyachi T, Ohara S, Matsumoto T (1998) Quantitative analysis of CSF flow dynamics using MRI in normal pressure hydrocephalus. Acta Neurochir Suppl 71:350–353PubMed
11.
go back to reference Bradley WG (2002) Cerebrospinal fluid dynamics and shunt responsiveness in patients with normal-pressure hydrocephalus. Mayo Clin Proc 77:507–508CrossRef Bradley WG (2002) Cerebrospinal fluid dynamics and shunt responsiveness in patients with normal-pressure hydrocephalus. Mayo Clin Proc 77:507–508CrossRef
12.
go back to reference Jurcoane A, Keil F, Szelenyi A, Pfeilschifter W, Singer OC, Hattingen E (2014) Directional diffusion of corticospinal tract supports therapy decisions in idiopathic normal-pressure hydrocephalusjm. Neuroradiology 56:5–13CrossRef Jurcoane A, Keil F, Szelenyi A, Pfeilschifter W, Singer OC, Hattingen E (2014) Directional diffusion of corticospinal tract supports therapy decisions in idiopathic normal-pressure hydrocephalusjm. Neuroradiology 56:5–13CrossRef
13.
go back to reference Hattori T, Yuasa T, Aoki S et al (2011) Altered microstructure in corticospinal tract in idiopathic normal pressure hydrocephalus: comparison with Alzheimer disease and Parkinson disease with dementia. AJNR Am J Neuroradiol 32:1681–1687CrossRef Hattori T, Yuasa T, Aoki S et al (2011) Altered microstructure in corticospinal tract in idiopathic normal pressure hydrocephalus: comparison with Alzheimer disease and Parkinson disease with dementia. AJNR Am J Neuroradiol 32:1681–1687CrossRef
14.
go back to reference Planetta PJ, Schulze ET, Geary EK et al (2013) Thalamic projection fiber integrity in de novo Parkinson disease. AJNR Am J Neuroradiol 34:74–79CrossRef Planetta PJ, Schulze ET, Geary EK et al (2013) Thalamic projection fiber integrity in de novo Parkinson disease. AJNR Am J Neuroradiol 34:74–79CrossRef
15.
go back to reference Mole JP, Subramanian L, Bracht T, Morris H, Metzler-Baddeley C, Linden DE (2016) Increased fractional anisotropy in the motor tracts of Parkinson's disease suggests compensatory neuroplasticity or selective neurodegeneration. Eur Radiol 26:3327–3335CrossRef Mole JP, Subramanian L, Bracht T, Morris H, Metzler-Baddeley C, Linden DE (2016) Increased fractional anisotropy in the motor tracts of Parkinson's disease suggests compensatory neuroplasticity or selective neurodegeneration. Eur Radiol 26:3327–3335CrossRef
16.
go back to reference Krupa DJ, Ghazanfar AA, Nicolelis MA (1999) Immediate thalamic sensory plasticity depends on corticothalamic feedback. Proc Natl Acad Sci U S A 96:8200–8205CrossRef Krupa DJ, Ghazanfar AA, Nicolelis MA (1999) Immediate thalamic sensory plasticity depends on corticothalamic feedback. Proc Natl Acad Sci U S A 96:8200–8205CrossRef
18.
go back to reference Sommer MA (2003) The role of the thalamus in motor control. Curr Opin Neurobiol 13:663–670CrossRef Sommer MA (2003) The role of the thalamus in motor control. Curr Opin Neurobiol 13:663–670CrossRef
19.
go back to reference Ishikawa M, Hashimoto M, Kuwana N et al (2008) Guidelines for management of idiopathic normal pressure hydrocephalus. Neurol Med Chir (Tokyo) 48:S1–S23CrossRef Ishikawa M, Hashimoto M, Kuwana N et al (2008) Guidelines for management of idiopathic normal pressure hydrocephalus. Neurol Med Chir (Tokyo) 48:S1–S23CrossRef
20.
go back to reference Huang TY, Chung HW, Chen MY et al (2004) Supratentorial cerebrospinal fluid production rate in healthy adults: quantification with two-dimensional cine phase-contrast MR imaging with high temporal and spatial resolution. Radiology 233:603–608CrossRef Huang TY, Chung HW, Chen MY et al (2004) Supratentorial cerebrospinal fluid production rate in healthy adults: quantification with two-dimensional cine phase-contrast MR imaging with high temporal and spatial resolution. Radiology 233:603–608CrossRef
21.
go back to reference Lee JH, Lee HK, Kim JK, Kim HJ, Park JK, Choi CG (2004) CSF flow quantification of the cerebral aqueduct in normal volunteers using phase contrast cine MR imaging. Korean J Radiol 5:81–86CrossRef Lee JH, Lee HK, Kim JK, Kim HJ, Park JK, Choi CG (2004) CSF flow quantification of the cerebral aqueduct in normal volunteers using phase contrast cine MR imaging. Korean J Radiol 5:81–86CrossRef
22.
go back to reference Le Bihan D, Mangin JF, Poupon C et al (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13:534–546CrossRef Le Bihan D, Mangin JF, Poupon C et al (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13:534–546CrossRef
23.
go back to reference Tournier JD, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fibre regions. Int J Imaging Syst Technol 22:53–66CrossRef Tournier JD, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fibre regions. Int J Imaging Syst Technol 22:53–66CrossRef
24.
go back to reference Yamada K, Akazawa K, Yuen S et al (2010) MR imaging of ventral thalamic nuclei. AJNR Am J Neuroradiol 31:732–735CrossRef Yamada K, Akazawa K, Yuen S et al (2010) MR imaging of ventral thalamic nuclei. AJNR Am J Neuroradiol 31:732–735CrossRef
25.
go back to reference Seo JP, Jang SH (2013) Different characteristics of the corticospinal tract according to the cerebral origin: DTI study. AJNR Am J Neuroradiol 34:1359–1363CrossRef Seo JP, Jang SH (2013) Different characteristics of the corticospinal tract according to the cerebral origin: DTI study. AJNR Am J Neuroradiol 34:1359–1363CrossRef
26.
go back to reference Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate a practical and powerful approach to multiple testing. J R Stat Soc Series B 57:289–300 Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate a practical and powerful approach to multiple testing. J R Stat Soc Series B 57:289–300
27.
go back to reference Morgante F, Naro A, Terranova C et al (2017) Normal sensorimotor plasticity in complex regional pain syndrome with fixed posture of the hand. Mov Disord 32:149–157CrossRef Morgante F, Naro A, Terranova C et al (2017) Normal sensorimotor plasticity in complex regional pain syndrome with fixed posture of the hand. Mov Disord 32:149–157CrossRef
28.
go back to reference Audoin B, Guye M, Reuter F et al (2007) Structure of WM bundles constituting the working memory system in early multiple sclerosis: a quantitative DTI tractography study. Neuroimage 36:1324–1330CrossRef Audoin B, Guye M, Reuter F et al (2007) Structure of WM bundles constituting the working memory system in early multiple sclerosis: a quantitative DTI tractography study. Neuroimage 36:1324–1330CrossRef
29.
go back to reference Juottonen K, Gockel M, Silén T, Hurri H, Hari R, Forss N (2002) Altered central sensorimotor processing in patients with complex regional pain syndrome. Pain 98:315–323CrossRef Juottonen K, Gockel M, Silén T, Hurri H, Hari R, Forss N (2002) Altered central sensorimotor processing in patients with complex regional pain syndrome. Pain 98:315–323CrossRef
30.
go back to reference Xu J, Li H, Harkins KD et al (2014) Mapping mean axon diameter and axonal volume fraction by MRI using temporal diffusion spectroscopy. Neuroimage 103:10–19CrossRef Xu J, Li H, Harkins KD et al (2014) Mapping mean axon diameter and axonal volume fraction by MRI using temporal diffusion spectroscopy. Neuroimage 103:10–19CrossRef
31.
go back to reference Tovar-Moll F, Evangelou IE, Chiu AW et al (2009) Thalamic involvement and its impact on clinical disability in patients with multiple sclerosis: a diffusion tensor imaging study at 3T. AJNR Am J Neuroradiol 30:1380–1386CrossRef Tovar-Moll F, Evangelou IE, Chiu AW et al (2009) Thalamic involvement and its impact on clinical disability in patients with multiple sclerosis: a diffusion tensor imaging study at 3T. AJNR Am J Neuroradiol 30:1380–1386CrossRef
32.
go back to reference Macchi G, Jones EG (1997) Toward an agreement on terminology of nuclear and subnuclear divisions of the motor thalamus. J Neurosurg 86:77–92CrossRef Macchi G, Jones EG (1997) Toward an agreement on terminology of nuclear and subnuclear divisions of the motor thalamus. J Neurosurg 86:77–92CrossRef
34.
go back to reference Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev 31:236–250CrossRef Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev 31:236–250CrossRef
35.
go back to reference Siegfried J, Lippitz B (1994) Chronic electrical stimulation of the VL-VPL complex and of the pallidum in the treatment of movement disorders: personal experience since 1982. Stereotact Funct Neurosurg 62:71–75CrossRef Siegfried J, Lippitz B (1994) Chronic electrical stimulation of the VL-VPL complex and of the pallidum in the treatment of movement disorders: personal experience since 1982. Stereotact Funct Neurosurg 62:71–75CrossRef
36.
go back to reference Alomar S, King NK, Tam J, Bari AA, Hamani C, Lozano AM (2017) Speech and language adverse effects after thalamotomy and deep brain stimulation in patients with movement disorders: A meta-analysis. Mov Disord 32:53–63CrossRef Alomar S, King NK, Tam J, Bari AA, Hamani C, Lozano AM (2017) Speech and language adverse effects after thalamotomy and deep brain stimulation in patients with movement disorders: A meta-analysis. Mov Disord 32:53–63CrossRef
37.
go back to reference Fasano A, Herzog J, Raethjen J et al (2010) Gait ataxia in essential tremor is differentially modulated by thalamic stimulation. Brain 133:3635–3648CrossRef Fasano A, Herzog J, Raethjen J et al (2010) Gait ataxia in essential tremor is differentially modulated by thalamic stimulation. Brain 133:3635–3648CrossRef
Metadata
Title
Changes in sensorimotor-related thalamic diffusion properties and cerebrospinal fluid hydrodynamics predict gait responses to tap test in idiopathic normal-pressure hydrocephalus
Authors
Ping-Huei Tsai
Yung-Chieh Chen
Shih-Wei Chiang
Teng-Yi Huang
Ming-Chung Chou
Hua-Shan Liu
Hsiao-Wen Chung
Giia-Sheun Peng
Hsin-I Ma
Hung-Wen Kao
Cheng-Yu Chen
Publication date
01-11-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 11/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5488-x

Other articles of this Issue 11/2018

European Radiology 11/2018 Go to the issue