Skip to main content
Top
Published in: Fluids and Barriers of the CNS 1/2018

Open Access 01-12-2018 | Research

Paradigm-shift: radiological changes in the asymptomatic iNPH-patient to be: an observational study

Authors: D. C. Engel, S. D. Adib, M. U. Schuhmann, C. Brendle

Published in: Fluids and Barriers of the CNS | Issue 1/2018

Login to get access

Abstract

Background

Many radiological signs are known for the diagnosis of idiopathic normal pressure hydrocephalus (iNPH). However, there is little information about these signs in the pre-symptomatic phase. For pathophysiological investigative purposes we conducted a descriptive image analysis study on pre-symptomatic patients.

Methods

Patients that had contact with either the neurological or neurosurgical department of the university hospital Tuebingen from 2010 through 2016 with magnetic resonance images > 3 years before onset of symptoms, were included. The date of onset and severity of symptoms, date of first imaging and birth date were recorded. Evan’s index (EI), width of the third ventricle (3VW), tight high convexity (THC), Sylvian fissure, extent of white matter hyperintensities and aqueductal flow were assessed in images before and around symptom onset.

Results

Ten patients were included. In all ten patients the first symptom was gait disturbance. Nine of ten pre-symptomatic images showed classic signs for iNPH. EI showed a significant increase between the pre-symptomatic and symptomatic phase. 3VW showed a trend for increase without significance. THC changed back and forth over time within some patients.

Conclusions

In accordance with the scarce literature available, radiological changes are present at least 3 years before onset of iNPH-symptoms. EI seems to be a robust measure for pre-symptomatic radiological changes. Extrapolating the data, the development of iNPH typical changes might be an insidious process and the development of THC might be a variable and non-linear process. Further studies with larger sample sizes are necessary to put these findings into the pathophysiological perspective for the development of iNPH.
Literature
1.
go back to reference Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH. Symptomatic occult hydrocephalus normal cerebrospinal-fluid pressure. A treatable syndrome. N Engl J Med. 1965;273:117–26.CrossRefPubMed Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH. Symptomatic occult hydrocephalus normal cerebrospinal-fluid pressure. A treatable syndrome. N Engl J Med. 1965;273:117–26.CrossRefPubMed
2.
go back to reference Kuriyama N, Miyajima M, Nakajima M, Kurosawa M, Fukushima W, Watanabe Y, et al. Nationwide hospital-based survey of idiopathic normal pressure hydrocephalus in Japan: epidemiological and clinical characteristics. Brain Behav. 2017;7:e00635.CrossRefPubMedPubMedCentral Kuriyama N, Miyajima M, Nakajima M, Kurosawa M, Fukushima W, Watanabe Y, et al. Nationwide hospital-based survey of idiopathic normal pressure hydrocephalus in Japan: epidemiological and clinical characteristics. Brain Behav. 2017;7:e00635.CrossRefPubMedPubMedCentral
3.
go back to reference Brean A, Eide PK. Prevalence of probable idiopathic normal pressure hydrocephalus in a Norwegian population. Acta Neurol Scand. 2008;118:48–53.CrossRefPubMed Brean A, Eide PK. Prevalence of probable idiopathic normal pressure hydrocephalus in a Norwegian population. Acta Neurol Scand. 2008;118:48–53.CrossRefPubMed
4.
5.
go back to reference Iseki C, Takahashi Y, Wada M, Kawanami T, Adachi M, Kato T. Incidence of idiopathic normal pressure hydrocephalus (iNPH): a 10-year follow-up study of a rural community in Japan. J Neurol Sci. 2014;339:108–12.CrossRefPubMed Iseki C, Takahashi Y, Wada M, Kawanami T, Adachi M, Kato T. Incidence of idiopathic normal pressure hydrocephalus (iNPH): a 10-year follow-up study of a rural community in Japan. J Neurol Sci. 2014;339:108–12.CrossRefPubMed
6.
go back to reference Wilson RK, Williams MA. Evidence that congenital hydrocephalus is a precursor to idiopathic normal pressure hydrocephalus in only a subset of patients. J Neurol Neurosurg Psychiatry. 2007;78:508–11.CrossRefPubMedPubMedCentral Wilson RK, Williams MA. Evidence that congenital hydrocephalus is a precursor to idiopathic normal pressure hydrocephalus in only a subset of patients. J Neurol Neurosurg Psychiatry. 2007;78:508–11.CrossRefPubMedPubMedCentral
7.
go back to reference Bradley WG, Safar FG, Hurtado C, Ord J, Alksne JF. Increased intracranial volume: a clue to the etiology of idiopathic normal-pressure hydrocephalus? Am J Neuroradiol. 2004;25:1479–84.PubMed Bradley WG, Safar FG, Hurtado C, Ord J, Alksne JF. Increased intracranial volume: a clue to the etiology of idiopathic normal-pressure hydrocephalus? Am J Neuroradiol. 2004;25:1479–84.PubMed
8.
go back to reference Nakano H, Bandoh K, Miyaoka M, Sato K. Evaluation of hydrocephalic periventricular radiolucency by dynamic computed tomography and xenon-computed tomography. Neurosurgery. 1996;39:758–63.CrossRefPubMed Nakano H, Bandoh K, Miyaoka M, Sato K. Evaluation of hydrocephalic periventricular radiolucency by dynamic computed tomography and xenon-computed tomography. Neurosurgery. 1996;39:758–63.CrossRefPubMed
9.
go back to reference Qvarlander S, Ambarki K, Wåhlin A, Jacobsson J, Birgander R, Malm J, et al. Cerebrospinal fluid and blood flow patterns in idiopathic normal pressure hydrocephalus. Acta Neurol Scand. 2017;135:576–84.CrossRefPubMed Qvarlander S, Ambarki K, Wåhlin A, Jacobsson J, Birgander R, Malm J, et al. Cerebrospinal fluid and blood flow patterns in idiopathic normal pressure hydrocephalus. Acta Neurol Scand. 2017;135:576–84.CrossRefPubMed
10.
go back to reference Kuriyama N, Tokuda T, Yamada K, Akazawa K, Hosoda M, Sakai K, et al. Flow velocity of the superior sagittal sinus is reduced in patients with idiopathic normal pressure hydrocephalus. J Neuroimaging. 2011;21:365–9.CrossRefPubMed Kuriyama N, Tokuda T, Yamada K, Akazawa K, Hosoda M, Sakai K, et al. Flow velocity of the superior sagittal sinus is reduced in patients with idiopathic normal pressure hydrocephalus. J Neuroimaging. 2011;21:365–9.CrossRefPubMed
11.
go back to reference Kuriyama N, Tokuda T, Miyamoto J, Takayasu N, Kondo M, Nakagawa M. Retrograde jugular flow associated with idiopathic normal pressure hydrocephalus. Ann Neurol. 2008;64:217–21.CrossRefPubMed Kuriyama N, Tokuda T, Miyamoto J, Takayasu N, Kondo M, Nakagawa M. Retrograde jugular flow associated with idiopathic normal pressure hydrocephalus. Ann Neurol. 2008;64:217–21.CrossRefPubMed
12.
go back to reference El Sankari S, Fichten A, Gondry-Jouet C, Czosnyka M, Legars D, Deramond H, et al. Correlation between tap test and CSF aqueductal stroke volume in idiopathic normal pressure hydrocephalus. Acta Neurochir Suppl. 2012;113:43–6.CrossRefPubMed El Sankari S, Fichten A, Gondry-Jouet C, Czosnyka M, Legars D, Deramond H, et al. Correlation between tap test and CSF aqueductal stroke volume in idiopathic normal pressure hydrocephalus. Acta Neurochir Suppl. 2012;113:43–6.CrossRefPubMed
13.
go back to reference Ringstad G, Emblem KE, Eide PK. Phase-contrast magnetic resonance imaging reveals net retrograde aqueductal flow in idiopathic normal pressure hydrocephalus. J Neurosurg. 2015;1–8. Ringstad G, Emblem KE, Eide PK. Phase-contrast magnetic resonance imaging reveals net retrograde aqueductal flow in idiopathic normal pressure hydrocephalus. J Neurosurg. 2015;1–8.
14.
go back to reference Eklund A, Smielewski P, Chambers I, Alperin N, Malm J, Czosnyka M, et al. Assessment of cerebrospinal fluid outflow resistance. Med Biol Eng Comput. 2007;45:719–35.CrossRefPubMed Eklund A, Smielewski P, Chambers I, Alperin N, Malm J, Czosnyka M, et al. Assessment of cerebrospinal fluid outflow resistance. Med Biol Eng Comput. 2007;45:719–35.CrossRefPubMed
15.
go back to reference Qvarlander S, Lundkvist B, Koskinen L-OD, Malm J, Eklund A. Pulsatility in CSF dynamics: pathophysiology of idiopathic normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry. 2013;84:735–41.CrossRefPubMed Qvarlander S, Lundkvist B, Koskinen L-OD, Malm J, Eklund A. Pulsatility in CSF dynamics: pathophysiology of idiopathic normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry. 2013;84:735–41.CrossRefPubMed
16.
go back to reference Wikkelsø C, Hellström P, Klinge PM, Tans JTJ. The European iNPH Multicentre Study on the predictive values of resistance to CSF outflow and the CSF Tap Test in patients with idiopathic normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry. 2013;84:562–8.CrossRefPubMed Wikkelsø C, Hellström P, Klinge PM, Tans JTJ. The European iNPH Multicentre Study on the predictive values of resistance to CSF outflow and the CSF Tap Test in patients with idiopathic normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry. 2013;84:562–8.CrossRefPubMed
17.
go back to reference Kizu O, Yamada K, Nishimura T. Proton chemical shift imaging in normal pressure hydrocephalus. AJNR Am J Neuroradiol. 2001;22:1659–64.PubMed Kizu O, Yamada K, Nishimura T. Proton chemical shift imaging in normal pressure hydrocephalus. AJNR Am J Neuroradiol. 2001;22:1659–64.PubMed
18.
go back to reference Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM. Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005;57(3 Suppl):S4–16 (discussion ii–v).PubMed Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM. Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005;57(3 Suppl):S4–16 (discussion ii–v).PubMed
19.
go back to reference Alperin N, Oliu CJ, Bagci AM, Lee SH, Kovanlikaya I, Adams D, et al. Low-dose acetazolamide reverses periventricular white matter hyperintensities in iNPH. Neurology. 2014;82:1347–51.CrossRefPubMedPubMedCentral Alperin N, Oliu CJ, Bagci AM, Lee SH, Kovanlikaya I, Adams D, et al. Low-dose acetazolamide reverses periventricular white matter hyperintensities in iNPH. Neurology. 2014;82:1347–51.CrossRefPubMedPubMedCentral
20.
go back to reference Shinoda N, Hirai O, Hori S, Mikami K, Bando T, Shimo D, et al. Utility of MRI-based disproportionately enlarged subarachnoid space hydrocephalus scoring for predicting prognosis after surgery for idiopathic normal pressure hydrocephalus: clinical research. J Neurosurg. 2017;1–7. Shinoda N, Hirai O, Hori S, Mikami K, Bando T, Shimo D, et al. Utility of MRI-based disproportionately enlarged subarachnoid space hydrocephalus scoring for predicting prognosis after surgery for idiopathic normal pressure hydrocephalus: clinical research. J Neurosurg. 2017;1–7.
21.
go back to reference Pyykkö OT, Lumela M, Rummukainen J, Nerg O, Seppälä TT, Herukka S-K, et al. Cerebrospinal fluid biomarker and brain biopsy findings in idiopathic normal pressure hydrocephalus. PLoS ONE. 2014;9:e91974.CrossRefPubMedPubMedCentral Pyykkö OT, Lumela M, Rummukainen J, Nerg O, Seppälä TT, Herukka S-K, et al. Cerebrospinal fluid biomarker and brain biopsy findings in idiopathic normal pressure hydrocephalus. PLoS ONE. 2014;9:e91974.CrossRefPubMedPubMedCentral
22.
go back to reference Tullberg M, Rosengren L, Blomsterwall E, Karlsson JE, Wikkelsö C. CSF neurofilament and glial fibrillary acidic protein in normal pressure hydrocephalus. Neurology. 1998;50:1122–7.CrossRefPubMed Tullberg M, Rosengren L, Blomsterwall E, Karlsson JE, Wikkelsö C. CSF neurofilament and glial fibrillary acidic protein in normal pressure hydrocephalus. Neurology. 1998;50:1122–7.CrossRefPubMed
23.
go back to reference 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;2:307–27.CrossRefPubMed 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;2:307–27.CrossRefPubMed
24.
go back to reference Eide PK, Sorteberg W. Diagnostic intracranial pressure monitoring and surgical management in idiopathic normal pressure hydrocephalus: a 6-Year review of 214 patients. Neurosurgery. 2010;66:80–90.CrossRefPubMed Eide PK, Sorteberg W. Diagnostic intracranial pressure monitoring and surgical management in idiopathic normal pressure hydrocephalus: a 6-Year review of 214 patients. Neurosurgery. 2010;66:80–90.CrossRefPubMed
25.
go back to reference Miyake H, Ohta T, Kajimoto Y, Deguchi J. Diamox® challenge test to decide indications for cerebrospinal fluid shunting in normal pressure hydrocephalus. Acta Neurochir (Wien). 1999;141:1187–93.CrossRefPubMed Miyake H, Ohta T, Kajimoto Y, Deguchi J. Diamox® challenge test to decide indications for cerebrospinal fluid shunting in normal pressure hydrocephalus. Acta Neurochir (Wien). 1999;141:1187–93.CrossRefPubMed
26.
go back to reference Tanaka A, Kimura M, Nakayama Y, Yoshinaga S, Tomonaga M. Cerebral blood flow and autoregulation in normal pressure hydrocephalus. Neurosurgery. 1997;40:1165–7.CrossRef Tanaka A, Kimura M, Nakayama Y, Yoshinaga S, Tomonaga M. Cerebral blood flow and autoregulation in normal pressure hydrocephalus. Neurosurgery. 1997;40:1165–7.CrossRef
27.
go back to reference Rekate HL, Brodkey JA, Chizeck HJ, el Sakka W, Ko WH. Ventricular volume regulation: a mathematical model and computer simulation. Pediatr Neurosci. 1988;14:77–84.CrossRefPubMed Rekate HL, Brodkey JA, Chizeck HJ, el Sakka W, Ko WH. Ventricular volume regulation: a mathematical model and computer simulation. Pediatr Neurosci. 1988;14:77–84.CrossRefPubMed
28.
go back to reference Bradley WG. Diagnostic tools in hydrocephalus. Neurosurg Clin N Am. 2001;12:661–84 (viii).PubMed Bradley WG. Diagnostic tools in hydrocephalus. Neurosurg Clin N Am. 2001;12:661–84 (viii).PubMed
29.
go back to reference Bradley WG. Cerebrospinal fluid dynamics and shunt responsiveness in patients with normal-pressure hydrocephalus. Mayo Clin Proc. 2002;77:507–8.CrossRefPubMed Bradley WG. Cerebrospinal fluid dynamics and shunt responsiveness in patients with normal-pressure hydrocephalus. Mayo Clin Proc. 2002;77:507–8.CrossRefPubMed
30.
go back to reference Greitz D. Radiological assessment of hydrocephalus: new theories and implications for therapy. Neurosurg Rev. 2004;27:145–65.PubMed Greitz D. Radiological assessment of hydrocephalus: new theories and implications for therapy. Neurosurg Rev. 2004;27:145–65.PubMed
31.
go back to reference Greitz D. Cerebrospinal fluid circulation and associated intracranial dynamics. A radiologic investigation using MR imaging and radionuclide cisternography. Acta Radiol Suppl. 1993;386:1–23.PubMed Greitz D. Cerebrospinal fluid circulation and associated intracranial dynamics. A radiologic investigation using MR imaging and radionuclide cisternography. Acta Radiol Suppl. 1993;386:1–23.PubMed
32.
go back to reference Jeppsson A, Zetterberg H, Blennow K, Wikkelsø C. Idiopathic normal-pressure hydrocephalus: pathophysiology and diagnosis by CSF biomarkers. Neurology. 2013;80:1385–92.CrossRefPubMed Jeppsson A, Zetterberg H, Blennow K, Wikkelsø C. Idiopathic normal-pressure hydrocephalus: pathophysiology and diagnosis by CSF biomarkers. Neurology. 2013;80:1385–92.CrossRefPubMed
33.
go back to reference Cusimano MD, Rewilak D, Stuss DT, Barrera-Martinez JC, Salehi F, Freedman M. Normal-pressure hydrocephalus: is there a genetic predisposition? Can J Neurol Sci. 2011;38:274–81.CrossRefPubMed Cusimano MD, Rewilak D, Stuss DT, Barrera-Martinez JC, Salehi F, Freedman M. Normal-pressure hydrocephalus: is there a genetic predisposition? Can J Neurol Sci. 2011;38:274–81.CrossRefPubMed
34.
go back to reference Huovinen J, Kastinen S, Komulainen S, Oinas M, Avellan C, Frantzen J, et al. Familial idiopathic normal pressure hydrocephalus. J Neurol Sci. 2016;368:11–8.CrossRefPubMed Huovinen J, Kastinen S, Komulainen S, Oinas M, Avellan C, Frantzen J, et al. Familial idiopathic normal pressure hydrocephalus. J Neurol Sci. 2016;368:11–8.CrossRefPubMed
35.
go back to reference Takahashi Y, Kawanami T, Nagasawa H, Iseki C, Hanyu H, Kato T. Familial normal pressure hydrocephalus (NPH) with an autosomal-dominant inheritance: a novel subgroup of NPH. J Neurol Sci. 2011;308:149–51.CrossRefPubMed Takahashi Y, Kawanami T, Nagasawa H, Iseki C, Hanyu H, Kato T. Familial normal pressure hydrocephalus (NPH) with an autosomal-dominant inheritance: a novel subgroup of NPH. J Neurol Sci. 2011;308:149–51.CrossRefPubMed
36.
go back to reference Stolze H, Kuhtz-Buschbeck JP, Drücke H, Jöhnk K, Diercks C, Palmié S, et al. Gait analysis in idiopathic normal pressure hydrocephalus—which parameters respond to the CSF tap test? Clin Neurophysiol. 2000;111:1678–86.CrossRefPubMed Stolze H, Kuhtz-Buschbeck JP, Drücke H, Jöhnk K, Diercks C, Palmié S, et al. Gait analysis in idiopathic normal pressure hydrocephalus—which parameters respond to the CSF tap test? Clin Neurophysiol. 2000;111:1678–86.CrossRefPubMed
37.
38.
go back to reference Tolze H, Kuhtz-Buschbeck JP, Drücke H, Jöhnk K, Illert M, Deuschl G. Comparative analysis of the gait disorder of normal pressure hydrocephalus and Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2001;70:289–97.CrossRef Tolze H, Kuhtz-Buschbeck JP, Drücke H, Jöhnk K, Illert M, Deuschl G. Comparative analysis of the gait disorder of normal pressure hydrocephalus and Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2001;70:289–97.CrossRef
39.
go back to reference Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM. INPH guidelines, part II: diagnosing idio-pathic normal-pressure hydrocephalus. Neurosurgery. 2005;57(3 SUPPL):S2–17. Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM. INPH guidelines, part II: diagnosing idio-pathic normal-pressure hydrocephalus. Neurosurgery. 2005;57(3 SUPPL):S2–17.
40.
go back to reference Evans WA, Davidoff LM, Dyke CG, King GC. An encephalographic ratio for estimating ventricular enlargement and cerebral atrophy. Arch Neurol Psychiatry. 1942;47:931.CrossRef Evans WA, Davidoff LM, Dyke CG, King GC. An encephalographic ratio for estimating ventricular enlargement and cerebral atrophy. Arch Neurol Psychiatry. 1942;47:931.CrossRef
41.
go back to reference Narita W, Nishio Y, Baba T, Iizuka O, Ishihara T, Matsuda M, et al. High-convexity tightness predicts the shunt response in idiopathic normal pressure hydrocephalus. Am J Neuroradiol. 2016;37:1831–7.CrossRef Narita W, Nishio Y, Baba T, Iizuka O, Ishihara T, Matsuda M, et al. High-convexity tightness predicts the shunt response in idiopathic normal pressure hydrocephalus. Am J Neuroradiol. 2016;37:1831–7.CrossRef
42.
go back to reference Fazekas F, Chawluk JB, Alavi A. MR signal abnormalities at 1.5 T in alzheimer’s dementia and normal aging. Am J Neuroradiol. 1987;8:421–6. Fazekas F, Chawluk JB, Alavi A. MR signal abnormalities at 1.5 T in alzheimer’s dementia and normal aging. Am J Neuroradiol. 1987;8:421–6.
43.
go back to reference Bradley WG. CSF Flow in the brain in the context of normal pressure hydrocephalus. AJNR Am J Neuroradiol. 2015;36:831–8.CrossRefPubMed Bradley WG. CSF Flow in the brain in the context of normal pressure hydrocephalus. AJNR Am J Neuroradiol. 2015;36:831–8.CrossRefPubMed
44.
go back to reference Eide PK, Saehle T. Is ventriculomegaly in idiopathic normal pressure hydrocephalus associated with a transmantle gradient in pulsatile intracranial pressure? Acta Neurochir (Wien). 2010;152:989–95.CrossRefPubMed Eide PK, Saehle T. Is ventriculomegaly in idiopathic normal pressure hydrocephalus associated with a transmantle gradient in pulsatile intracranial pressure? Acta Neurochir (Wien). 2010;152:989–95.CrossRefPubMed
45.
go back to reference Greitz D. New view on the CSF circulation: CSF is produced and absorbed by brain capillaries. Neuroradiol J. 2010;23:94–5. Greitz D. New view on the CSF circulation: CSF is produced and absorbed by brain capillaries. Neuroradiol J. 2010;23:94–5.
46.
go back to reference Burt VL, Whelton P, Roccella EJ, Brown C, Cutler JA, Higgins M, et al. Prevalence of hypertension in the US adult population. Results from the Third National Health and Nutrition Examination Survey, 1988–1991. Hypertension. 1995;25:305–13.CrossRefPubMed Burt VL, Whelton P, Roccella EJ, Brown C, Cutler JA, Higgins M, et al. Prevalence of hypertension in the US adult population. Results from the Third National Health and Nutrition Examination Survey, 1988–1991. Hypertension. 1995;25:305–13.CrossRefPubMed
47.
go back to reference Neuhauser HK, Adler C, Rosario AS, Diederichs C, Ellert U. Hypertension prevalence, awareness, treatment and control in Germany 1998 and 2008–11. J Hum Hypertens. 2015; August:1–7. Neuhauser HK, Adler C, Rosario AS, Diederichs C, Ellert U. Hypertension prevalence, awareness, treatment and control in Germany 1998 and 2008–11. J Hum Hypertens. 2015; August:1–7.
48.
go back to reference Akai K, Uchigasaki S, Tanaka U, Komatsu A. Normal pressure hydrocephalus, neuropathological study. Acta Pathol Jpn. 1987;37:97–110.PubMed Akai K, Uchigasaki S, Tanaka U, Komatsu A. Normal pressure hydrocephalus, neuropathological study. Acta Pathol Jpn. 1987;37:97–110.PubMed
49.
go back to reference Newton H, Pickard JD, Weller RO. Normal pressure hydrocephalus and cerebrovascular disease: findings of postmortem. J Neurol Neurosurg Psychiatry. 1989;52:804.CrossRefPubMedPubMedCentral Newton H, Pickard JD, Weller RO. Normal pressure hydrocephalus and cerebrovascular disease: findings of postmortem. J Neurol Neurosurg Psychiatry. 1989;52:804.CrossRefPubMedPubMedCentral
50.
go back to reference Bech RA, Waldemar G, Gjerris F, Klinken L, Juhler M. Shunting effects in patients with idiopathic normal pressure hydrocephalus; correlation with cerebral and leptomeningeal biopsy findings. Acta Neurochir (Wien). 1999;141:633–9.CrossRefPubMed Bech RA, Waldemar G, Gjerris F, Klinken L, Juhler M. Shunting effects in patients with idiopathic normal pressure hydrocephalus; correlation with cerebral and leptomeningeal biopsy findings. Acta Neurochir (Wien). 1999;141:633–9.CrossRefPubMed
51.
go back to reference Zarrinkoob L, Ambarki K, Wåhlin A, Birgander R, Carlberg B, Eklund A, et al. Aging alters the dampening of pulsatile blood flow in cerebral arteries. J Cereb Blood Flow Metab. 2016;36:1519–27.CrossRefPubMedPubMedCentral Zarrinkoob L, Ambarki K, Wåhlin A, Birgander R, Carlberg B, Eklund A, et al. Aging alters the dampening of pulsatile blood flow in cerebral arteries. J Cereb Blood Flow Metab. 2016;36:1519–27.CrossRefPubMedPubMedCentral
52.
go back to reference Swenson ER. Pharmacology of acute mountain sickness: old drugs and newer thinking. J Appl Physiol. 2016;120:204–15.CrossRefPubMed Swenson ER. Pharmacology of acute mountain sickness: old drugs and newer thinking. J Appl Physiol. 2016;120:204–15.CrossRefPubMed
53.
go back to reference Czosnyka Z, van den Boogaard F, Czosnyka M, Momjian S, Gelling L, Pickard JD. The relationship between CSF circulation and cerebrovascular pressure-reactivity in normal pressure hydrocephalus. Acta Neurochir Suppl. 2005;95:207–11.CrossRefPubMed Czosnyka Z, van den Boogaard F, Czosnyka M, Momjian S, Gelling L, Pickard JD. The relationship between CSF circulation and cerebrovascular pressure-reactivity in normal pressure hydrocephalus. Acta Neurochir Suppl. 2005;95:207–11.CrossRefPubMed
54.
go back to reference Yamada SM, Masahira N, Kawanishi Y, Fujimoto Y, Shimizu K. Preoperative acetazolamide SPECT is useful for predicting outcome of shunt operation in idiopathic normal pressure hydrocephalus patients. Clin Nucl Med. 2013;38:671–6.CrossRefPubMed Yamada SM, Masahira N, Kawanishi Y, Fujimoto Y, Shimizu K. Preoperative acetazolamide SPECT is useful for predicting outcome of shunt operation in idiopathic normal pressure hydrocephalus patients. Clin Nucl Med. 2013;38:671–6.CrossRefPubMed
55.
go back to reference Vakili S, Moran D, Hung A, Elder BD, Jeon L, Fialho H, et al. Timing of surgical treatment for idiopathic normal pressure hydrocephalus: association between treatment delay and reduced short-term benefit. Neurosurg Focus. 2016;41:E2.CrossRefPubMed Vakili S, Moran D, Hung A, Elder BD, Jeon L, Fialho H, et al. Timing of surgical treatment for idiopathic normal pressure hydrocephalus: association between treatment delay and reduced short-term benefit. Neurosurg Focus. 2016;41:E2.CrossRefPubMed
Metadata
Title
Paradigm-shift: radiological changes in the asymptomatic iNPH-patient to be: an observational study
Authors
D. C. Engel
S. D. Adib
M. U. Schuhmann
C. Brendle
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Fluids and Barriers of the CNS / Issue 1/2018
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/s12987-018-0090-9

Other articles of this Issue 1/2018

Fluids and Barriers of the CNS 1/2018 Go to the issue