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Published in: Fluids and Barriers of the CNS 1/2020

01-12-2020 | Central Nervous System Trauma | Research

Cerebrospinal fluid dynamics in non-acute post-traumatic ventriculomegaly

Authors: Afroditi D. Lalou, Virginia Levrini, Marek Czosnyka, Laurent Gergelé, Matthew Garnett, Angelos Kolias, Peter J. Hutchinson, Zofia Czosnyka

Published in: Fluids and Barriers of the CNS | Issue 1/2020

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Abstract

Background

Post-traumatic hydrocephalus (PTH) is potentially under-diagnosed and under-treated, generating the need for a more efficient diagnostic tool. We aim to report CSF dynamics of patients with post-traumatic ventriculomegaly.

Materials and methods

We retrospectively analysed post-traumatic brain injury (TBI) patients with ventriculomegaly who had undergone a CSF infusion test. We calculated the resistance to CSF outflow (Rout), AMP (pulse amplitude of intracranial pressure, ICP), dAMP (AMPplateau-AMPbaseline) and compensatory reserve index correlation coefficient between ICP and AMP (RAP). To avoid confounding factors, included patients had to be non-decompressed or with cranioplasty > 1 month previously and Rout > 6 mmHg/min/ml. Compliance was assessed using the elasticity coefficient. We also compared infusion-tested TBI patients selected for shunting versus those not selected for shunting (consultant decision based on clinical and radiological assessment and the infusion results). Finally, we used data from a group of shunted idiopathic Normal Pressure Hydrocephalus (iNPH) patients for comparison.

Results

Group A consisted of 36 patients with post-traumatic ventriculomegaly and Group B of 45 iNPH shunt responders. AMP and dAMP were significantly lower in Group A than B (0.55 ± 0.39 vs 1.02 ± 0.72; p < 0.01 and 1.58 ± 1.21 vs 2.76 ± 1.5; p < 0.01. RAP baseline was not significantly different between the two. Elasticity was higher than the normal limit in all groups (average 0.18 1/ml). Significantly higher Rout was present in those with probable PTH selected for shunting compared with unshunted. Mild/moderate hydrocephalus, ex-vacuo ventriculomegaly/encephalomalacia were inconsistently reported in PTH patients.

Conclusions

Rout and AMP were significantly lower in PTH compared to iNPH and did not always reflect the degree of hydrocephalus or atrophy reported on CT/MRI. Compliance appears reduced in PTH.
Literature
1.
go back to reference Marmarou A, Abd-Elfattah Foda MA, Bandoh K, Yoshihara M, Yamamoto T, Tsuji O, et al. Posttraumatic ventriculomegaly: hydrocephalus or atrophy? A new approach for diagnosis using CSF dynamics. J Neurosurg. 1996;85:1026–35.PubMedCrossRef Marmarou A, Abd-Elfattah Foda MA, Bandoh K, Yoshihara M, Yamamoto T, Tsuji O, et al. Posttraumatic ventriculomegaly: hydrocephalus or atrophy? A new approach for diagnosis using CSF dynamics. J Neurosurg. 1996;85:1026–35.PubMedCrossRef
2.
go back to reference Manet R, Payen JF, Guerin R, Martinez O, Hautefeuille S, Francony G, et al. Using external lumbar CSF drainage to treat communicating external hydrocephalus in adult patients after acute traumatic or non-traumatic brain injury. Acta Neurochir (Wien). 2017;159(10):2003–9.PubMedCrossRef Manet R, Payen JF, Guerin R, Martinez O, Hautefeuille S, Francony G, et al. Using external lumbar CSF drainage to treat communicating external hydrocephalus in adult patients after acute traumatic or non-traumatic brain injury. Acta Neurochir (Wien). 2017;159(10):2003–9.PubMedCrossRef
3.
5.
go back to reference De Bonis P, Pompucci A, Mangiola A, Rigante L, Anile C. Post-traumatic hydrocephalus after decompressive craniectomy: an underestimated risk factor. J Neurotrauma. 2010;27(11):1965–70.PubMedCrossRef De Bonis P, Pompucci A, Mangiola A, Rigante L, Anile C. Post-traumatic hydrocephalus after decompressive craniectomy: an underestimated risk factor. J Neurotrauma. 2010;27(11):1965–70.PubMedCrossRef
7.
go back to reference Choi I, Park HK, Chang JC, Cho SJ, Choi SK, Byun BJ. Clinical factors for the development of posttraumatic hydrocephalus after decompressive craniectomy. J Korean Neurosurg Soc. 2008;43(5):227–31.PubMedPubMedCentralCrossRef Choi I, Park HK, Chang JC, Cho SJ, Choi SK, Byun BJ. Clinical factors for the development of posttraumatic hydrocephalus after decompressive craniectomy. J Korean Neurosurg Soc. 2008;43(5):227–31.PubMedPubMedCentralCrossRef
8.
go back to reference Cooper DJ, Rosenfeld JV, Murray L, Arabi YM, Davis AR, D’Urso P, Kossmann T, Ponsford J, Seppelt I, Reilly PW. Decompressive craniectomy in diffuse traumatic brain injury. N Engl J Med. 2011;364:1493–502.PubMedCrossRef Cooper DJ, Rosenfeld JV, Murray L, Arabi YM, Davis AR, D’Urso P, Kossmann T, Ponsford J, Seppelt I, Reilly PW. Decompressive craniectomy in diffuse traumatic brain injury. N Engl J Med. 2011;364:1493–502.PubMedCrossRef
9.
go back to reference Fotakopoulos G, Tsianaka E, Siasios G, Vagkopoulos K, Fountas K. Posttraumatic hydrocephalus after decompressive craniectomy in 126 patients with severe traumatic brain injury. J Neurol Surg A Cent Eur Neurosurg. 2016;77(02):88–92.PubMed Fotakopoulos G, Tsianaka E, Siasios G, Vagkopoulos K, Fountas K. Posttraumatic hydrocephalus after decompressive craniectomy in 126 patients with severe traumatic brain injury. J Neurol Surg A Cent Eur Neurosurg. 2016;77(02):88–92.PubMed
10.
go back to reference Kant IMJ, Mutsaerts HJMM, Van Montfort SJT, Jaarsma-Coes MG, Witkamp TD, Winterer G, et al. The association between frailty and MRI features of cerebral small vessel disease. Sci Rep. 2019;9(1):11343.PubMedPubMedCentralCrossRef Kant IMJ, Mutsaerts HJMM, Van Montfort SJT, Jaarsma-Coes MG, Witkamp TD, Winterer G, et al. The association between frailty and MRI features of cerebral small vessel disease. Sci Rep. 2019;9(1):11343.PubMedPubMedCentralCrossRef
12.
go back to reference Czosnyka M, Pickard J. Clinical assessment of cerebrospinal fluid dynamics in hydrocephalus Guide to interpretation based on observational study. J Neurol Neurosurg Psychiatry. 2000;68(2):246–8.PubMedPubMedCentralCrossRef Czosnyka M, Pickard J. Clinical assessment of cerebrospinal fluid dynamics in hydrocephalus Guide to interpretation based on observational study. J Neurol Neurosurg Psychiatry. 2000;68(2):246–8.PubMedPubMedCentralCrossRef
13.
go back to reference Kowalski RG, Weintraub AH, Rubin BA, Gerber DJ, Olsen AJ. Impact of timing of ventriculoperitoneal shunt placement on outcome in posttraumatic hydrocephalus. J Neurosurg. 2019;130(February):406–17.CrossRef Kowalski RG, Weintraub AH, Rubin BA, Gerber DJ, Olsen AJ. Impact of timing of ventriculoperitoneal shunt placement on outcome in posttraumatic hydrocephalus. J Neurosurg. 2019;130(February):406–17.CrossRef
14.
go back to reference Mazzini L, Campini R, Angelino E, Rognone F, Pastore I, Oliveri G. Posttraumatic hydrocephalus: a clinical, neuroradiologic, and neuropsychologic assessment of long-term outcome. Arch Phys Med Rehabil. 2003;84(11):1637–41.PubMedCrossRef Mazzini L, Campini R, Angelino E, Rognone F, Pastore I, Oliveri G. Posttraumatic hydrocephalus: a clinical, neuroradiologic, and neuropsychologic assessment of long-term outcome. Arch Phys Med Rehabil. 2003;84(11):1637–41.PubMedCrossRef
15.
go back to reference Cartwright C, Igbaseimokumo U. Lumbar puncture opening pressure is not a reliable measure of intracranial pressure in children. J Child Neurol. 2015;30(2):170–3.PubMedCrossRef Cartwright C, Igbaseimokumo U. Lumbar puncture opening pressure is not a reliable measure of intracranial pressure in children. J Child Neurol. 2015;30(2):170–3.PubMedCrossRef
17.
go back to reference Owler BK, Fong KCS, Czosnyka Z. Importance of ICP monitoring in the investigation of CSF circulation disorders. Br J Neurosurg. 2001;15(5):439–40.PubMedCrossRef Owler BK, Fong KCS, Czosnyka Z. Importance of ICP monitoring in the investigation of CSF circulation disorders. Br J Neurosurg. 2001;15(5):439–40.PubMedCrossRef
18.
go back to reference Czosnyka Z, Czosnyka M, Owler B, Momjian S, Kasprowicz M, Schmidt EA, et al. Clinical testing of CSF circulation in hydrocephalus. Acta Neurochir Suppl. 2005;95:247–51.PubMedCrossRef Czosnyka Z, Czosnyka M, Owler B, Momjian S, Kasprowicz M, Schmidt EA, et al. Clinical testing of CSF circulation in hydrocephalus. Acta Neurochir Suppl. 2005;95:247–51.PubMedCrossRef
19.
go back to reference Kasprowicz M, Lalou DA, Czosnyka M, Garnett M, Czosnyka Z. Intracranial pressure, its components and cerebrospinal fluid pressure–volume compensation. Acta Neurol Scand. 2016;134(3):168–80.PubMedCrossRef Kasprowicz M, Lalou DA, Czosnyka M, Garnett M, Czosnyka Z. Intracranial pressure, its components and cerebrospinal fluid pressure–volume compensation. Acta Neurol Scand. 2016;134(3):168–80.PubMedCrossRef
20.
go back to reference Owler BK, Pena A, Momjian S, Czosnyka Z, Czosnyka M, Harris NG, et al. Changes in cerebral blood flow during cerebrospinal fluid pressure manipulation in patients with normal pressure hydrocephalus: a methodological study. J Cereb Blood Flow Metab. 2004;24:579–87.PubMedCrossRef Owler BK, Pena A, Momjian S, Czosnyka Z, Czosnyka M, Harris NG, et al. Changes in cerebral blood flow during cerebrospinal fluid pressure manipulation in patients with normal pressure hydrocephalus: a methodological study. J Cereb Blood Flow Metab. 2004;24:579–87.PubMedCrossRef
21.
go back to reference Timofeev I, Czosnyka M, Nortje J, Smielewski P, Kirkpatrick P, Gupta A, et al. Effect of decompressive craniectomy on intracranial pressure and cerebrospinal compensation following traumatic brain injury. J Neurosurg. 2008;108(1):66–73.PubMedCrossRef Timofeev I, Czosnyka M, Nortje J, Smielewski P, Kirkpatrick P, Gupta A, et al. Effect of decompressive craniectomy on intracranial pressure and cerebrospinal compensation following traumatic brain injury. J Neurosurg. 2008;108(1):66–73.PubMedCrossRef
22.
go back to reference Czosnyka M, Czosnyka ZH, Momjian S, Pickard JD. Cerebrospinal fluid dynamics. Physiol Meas. 2004;25:R51–76.PubMedCrossRef Czosnyka M, Czosnyka ZH, Momjian S, Pickard JD. Cerebrospinal fluid dynamics. Physiol Meas. 2004;25:R51–76.PubMedCrossRef
23.
go back to reference National Institute for Health and Care Excellence (NICE): intraventional procedures guidance [IPG263] 2008 National Institute for Health and Care Excellence (NICE): intraventional procedures guidance [IPG263] 2008
24.
go back to reference Kim DJ, Czosnyka Z, Keong N, Radolovich DK, Smielewski P, Sutcliffe MPF, et al. Index of cerebrospinal compensatory reserve in hydrocephalus. Neurosurgery. 2009;64(3):494–501.PubMedCrossRef Kim DJ, Czosnyka Z, Keong N, Radolovich DK, Smielewski P, Sutcliffe MPF, et al. Index of cerebrospinal compensatory reserve in hydrocephalus. Neurosurgery. 2009;64(3):494–501.PubMedCrossRef
25.
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(8):719–35.PubMedCrossRef 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(8):719–35.PubMedCrossRef
26.
go back to reference Zeiler FA, Donnelly J, Menon DK, Smielewski P, Hutchinson PJA, Czosnyka M. A Description of a new continuous physiological index in traumatic brain injury using the correlation between pulse amplitude of intracranial pressure and cerebral perfusion pressure. J Neurotrauma. 2017;35(7):963–74.CrossRef Zeiler FA, Donnelly J, Menon DK, Smielewski P, Hutchinson PJA, Czosnyka M. A Description of a new continuous physiological index in traumatic brain injury using the correlation between pulse amplitude of intracranial pressure and cerebral perfusion pressure. J Neurotrauma. 2017;35(7):963–74.CrossRef
27.
go back to reference Donnelly J, Czosnyka M, Adams H, Cardim D, Kolias AG, Zeiler FA, et al. Twenty-five years of intracranial pressure monitoring after severe traumatic brain injury: a retrospective, single-center analysis. Neurosurgery. 2019;85(1):E75–82.PubMedCrossRef Donnelly J, Czosnyka M, Adams H, Cardim D, Kolias AG, Zeiler FA, et al. Twenty-five years of intracranial pressure monitoring after severe traumatic brain injury: a retrospective, single-center analysis. Neurosurgery. 2019;85(1):E75–82.PubMedCrossRef
28.
go back to reference Lilja-Cyron A, Andresen M, Kelsen J, Andreasen TH, Fugleholm K, Juhler M. Long-term effect of decompressive craniectomy on intracranial pressure and possible implications for intracranial fluid movements. Neurosurgery. 2020;86(2):231–40.PubMedCrossRef Lilja-Cyron A, Andresen M, Kelsen J, Andreasen TH, Fugleholm K, Juhler M. Long-term effect of decompressive craniectomy on intracranial pressure and possible implications for intracranial fluid movements. Neurosurgery. 2020;86(2):231–40.PubMedCrossRef
31.
go back to reference Nabbanja E, Czosnyka M, Keong NC, Garnett M, Pickard JD, Lalou DA, et al. Is there a link between ICP-derived infusion test parameters and outcome after shunting in normal pressure hydrocephalus? Vol. 126, Acta Neurochirurgica, Supplementum. 2018. Nabbanja E, Czosnyka M, Keong NC, Garnett M, Pickard JD, Lalou DA, et al. Is there a link between ICP-derived infusion test parameters and outcome after shunting in normal pressure hydrocephalus? Vol. 126, Acta Neurochirurgica, Supplementum. 2018.
32.
go back to reference Juniewicz H, Kasprowicz M, Czosnyka M, Czosnyka Z, Gizewski S, Dzik M, et al. Analysis of intracranial pressure during and after the infusion test in patients with communicating hydrocephalus. Physiol Meas. 2005;26(6):1039–48.PubMedCrossRef Juniewicz H, Kasprowicz M, Czosnyka M, Czosnyka Z, Gizewski S, Dzik M, et al. Analysis of intracranial pressure during and after the infusion test in patients with communicating hydrocephalus. Physiol Meas. 2005;26(6):1039–48.PubMedCrossRef
33.
go back to reference Swallow DMA, Fellner N, Varsos GV, Czosnyka M, Smielewski P, Pickard JD, et al. Repeatability of cerebrospinal fluid constant rate infusion study. Acta Neurol Scand. 2014;130(2):131–8.PubMedCrossRef Swallow DMA, Fellner N, Varsos GV, Czosnyka M, Smielewski P, Pickard JD, et al. Repeatability of cerebrospinal fluid constant rate infusion study. Acta Neurol Scand. 2014;130(2):131–8.PubMedCrossRef
34.
go back to reference Czosnyka Z, Czosnyka M, Lavinio A, Keong N, Pickard JD. Clinical testing of CSF circulation. Eur J Anaesthesiol. 2008;25(SUPPL. 42):142–5.CrossRef Czosnyka Z, Czosnyka M, Lavinio A, Keong N, Pickard JD. Clinical testing of CSF circulation. Eur J Anaesthesiol. 2008;25(SUPPL. 42):142–5.CrossRef
35.
go back to reference Eisenträger A, Sobey I, Czosnyka M, Eisentrager AS, Czosnyka M. Parameter estimations for the cerebrospinal fluid infusion test. Math Med Biol. 2013;30(2):157–74.PubMedCrossRef Eisenträger A, Sobey I, Czosnyka M, Eisentrager AS, Czosnyka M. Parameter estimations for the cerebrospinal fluid infusion test. Math Med Biol. 2013;30(2):157–74.PubMedCrossRef
36.
go back to reference Børgesen SE, Albeck MJ, Gjerris F, Czosnyka M, Laniewski P. Computerized infusion test compared to steady pressure constant infusion test in measurement of resistance to CSF outflow. Acta Neurochir (Wien). 1992;119(1–4):12–6.PubMedCrossRef Børgesen SE, Albeck MJ, Gjerris F, Czosnyka M, Laniewski P. Computerized infusion test compared to steady pressure constant infusion test in measurement of resistance to CSF outflow. Acta Neurochir (Wien). 1992;119(1–4):12–6.PubMedCrossRef
37.
go back to reference Kim D-J, Eng M, Czosnyka Z, Ph D, Sci FM. Index of cerebrospinal fluid compensatory reserve in hydrocephalus. Neurosurgery. 2009;64:494–502.PubMedCrossRef Kim D-J, Eng M, Czosnyka Z, Ph D, Sci FM. Index of cerebrospinal fluid compensatory reserve in hydrocephalus. Neurosurgery. 2009;64:494–502.PubMedCrossRef
39.
go back to reference Czosnyka M, Batorski L, Roszkowski M, Tomaszewski J, Wocjan J, Walencik A, et al. Cerebrospinal compensation in hydrocephalic children. Child’s Nerv Syst. 1993;9(1):17–22.CrossRef Czosnyka M, Batorski L, Roszkowski M, Tomaszewski J, Wocjan J, Walencik A, et al. Cerebrospinal compensation in hydrocephalic children. Child’s Nerv Syst. 1993;9(1):17–22.CrossRef
40.
go back to reference Czosnyka M, Czosnyka ZH, Momjian S, Pickard JD. Cerebrospinal fluid dynamics. Physiol Meas. 2004;25(5):R51–76.PubMedCrossRef Czosnyka M, Czosnyka ZH, Momjian S, Pickard JD. Cerebrospinal fluid dynamics. Physiol Meas. 2004;25(5):R51–76.PubMedCrossRef
41.
go back to reference Czosnyka M, Hutchinson PJ, Balestreri M, Hiler M, Smielewski P, Pickard JD. Monitoring and interpretation of intracranial pressure after head injury. Acta Neurochir Suppl. 2006;96:114–8.PubMedCrossRef Czosnyka M, Hutchinson PJ, Balestreri M, Hiler M, Smielewski P, Pickard JD. Monitoring and interpretation of intracranial pressure after head injury. Acta Neurochir Suppl. 2006;96:114–8.PubMedCrossRef
42.
go back to reference Reinard K, Basheer A, Phillips S, Snyder A, Agarwal A, Jafari-Khouzani K, et al. Simple and reproducible linear measurements to determine ventricular enlargement in adults. Surg Neurol Int. 2015;6(1):59.PubMedPubMedCentralCrossRef Reinard K, Basheer A, Phillips S, Snyder A, Agarwal A, Jafari-Khouzani K, et al. Simple and reproducible linear measurements to determine ventricular enlargement in adults. Surg Neurol Int. 2015;6(1):59.PubMedPubMedCentralCrossRef
43.
44.
go back to reference Ekstedt J. CSF hydrodynamic studies in man. J Neurol Psychiatry. 1978;41:345–53.CrossRef Ekstedt J. CSF hydrodynamic studies in man. J Neurol Psychiatry. 1978;41:345–53.CrossRef
45.
go back to reference Czosnyka M, Maksymowicz W, Batorski L, Czosnyka W, Koszewski Z. Comparison between classic-differential and automatic shunt functioning on the basis of infusion tests. Acta Neurochir (Wien). 1990;106:1–8.PubMedCrossRef Czosnyka M, Maksymowicz W, Batorski L, Czosnyka W, Koszewski Z. Comparison between classic-differential and automatic shunt functioning on the basis of infusion tests. Acta Neurochir (Wien). 1990;106:1–8.PubMedCrossRef
47.
go back to reference Czosnyka M, Laniewski W, Batorski L, Zaworski W. Analysis of Intracranial Pressure Waveform During Infusion Test. Acta Neurochir (Wien). 1988;93(3–4):140–5.PubMedCrossRef Czosnyka M, Laniewski W, Batorski L, Zaworski W. Analysis of Intracranial Pressure Waveform During Infusion Test. Acta Neurochir (Wien). 1988;93(3–4):140–5.PubMedCrossRef
48.
go back to reference Kim D, Kasprowicz M, Carrera E. The monitoring of relative changes in compartmental compliances of brain. Physiol Meas. 2009;30(7):647–59.PubMedCrossRef Kim D, Kasprowicz M, Carrera E. The monitoring of relative changes in compartmental compliances of brain. Physiol Meas. 2009;30(7):647–59.PubMedCrossRef
50.
go back to reference Czosnyka M, Czosnyka ZH, Whitfield PC, Donovan T, Pickard JD. Age dependence of cerebrospinal pressure—volume compensation in patients with hydrocephalus. J Neurosurg. 2009;94(3):482–6.CrossRef Czosnyka M, Czosnyka ZH, Whitfield PC, Donovan T, Pickard JD. Age dependence of cerebrospinal pressure—volume compensation in patients with hydrocephalus. J Neurosurg. 2009;94(3):482–6.CrossRef
51.
go back to reference Eide PK, Sorteberg W. Association among intracranial compliance, intracranial pulse pressure amplitude and intracranial pressure in patients with intracranial bleeds. Neurol Res. 2007;29(8):798–802.PubMedCrossRef Eide PK, Sorteberg W. Association among intracranial compliance, intracranial pulse pressure amplitude and intracranial pressure in patients with intracranial bleeds. Neurol Res. 2007;29(8):798–802.PubMedCrossRef
53.
go back to reference Lalou A, Levrini V, Garnett M, Nabbanja E, Kim D, Gergele L, et al. Validation of Davson’s equation in patients suffering from idiopathic normal pressure hydrocephalus. Acta Neurochir. 2018;106(5):1097–103.CrossRef Lalou A, Levrini V, Garnett M, Nabbanja E, Kim D, Gergele L, et al. Validation of Davson’s equation in patients suffering from idiopathic normal pressure hydrocephalus. Acta Neurochir. 2018;106(5):1097–103.CrossRef
54.
go back to reference Czosnyka M, Smielewski P, Timofeev I, Lavinio A, Guazzo E, Hutchinson P, Pickard JD. Intracranial pressure: more than a number. Neurosurg Focus. 2007;22(M):5–11. Czosnyka M, Smielewski P, Timofeev I, Lavinio A, Guazzo E, Hutchinson P, Pickard JD. Intracranial pressure: more than a number. Neurosurg Focus. 2007;22(M):5–11.
56.
go back to reference Bech-Azeddine R, Gjerris F, Waldemar G, Czosnyka M, Juhler M. Intraventricular or lumbar infusion test in adult communicating hydrocephalus? Practical consequences and clinical outcome of shunt operation. Acta Neurochir (Wien). 2005;147(10):1027–36.PubMedCrossRef Bech-Azeddine R, Gjerris F, Waldemar G, Czosnyka M, Juhler M. Intraventricular or lumbar infusion test in adult communicating hydrocephalus? Practical consequences and clinical outcome of shunt operation. Acta Neurochir (Wien). 2005;147(10):1027–36.PubMedCrossRef
57.
go back to reference Borgesen SE, Gjerris F. The predictive value of conductance to outflow of CSF in normal pressure hydrocephalus. Brain. 1982;105:65–86.PubMedCrossRef Borgesen SE, Gjerris F. The predictive value of conductance to outflow of CSF in normal pressure hydrocephalus. Brain. 1982;105:65–86.PubMedCrossRef
58.
go back to reference Kojoukhova M, Koivisto AM, Korhonen R, Remes AM, Vanninen R, Soininen H, et al. Feasibility of radiological markers in idiopathic normal pressure hydrocephalus. Acta Neurochir (Wien). 2015;157(10):1709–19.PubMedCrossRef Kojoukhova M, Koivisto AM, Korhonen R, Remes AM, Vanninen R, Soininen H, et al. Feasibility of radiological markers in idiopathic normal pressure hydrocephalus. Acta Neurochir (Wien). 2015;157(10):1709–19.PubMedCrossRef
59.
go back to reference Toma AK, Holl E, Kitchen ND, Watkins LD. Evans’ index revisited: the need for an alternative in normal pressure hydrocephalus. Neurosurgery. 2011;68(4):939–44.PubMedCrossRef Toma AK, Holl E, Kitchen ND, Watkins LD. Evans’ index revisited: the need for an alternative in normal pressure hydrocephalus. Neurosurgery. 2011;68(4):939–44.PubMedCrossRef
Metadata
Title
Cerebrospinal fluid dynamics in non-acute post-traumatic ventriculomegaly
Authors
Afroditi D. Lalou
Virginia Levrini
Marek Czosnyka
Laurent Gergelé
Matthew Garnett
Angelos Kolias
Peter J. Hutchinson
Zofia Czosnyka
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Fluids and Barriers of the CNS / Issue 1/2020
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/s12987-020-00184-6

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