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Open Access 01-12-2023 | Hydrocephalus | Research

Diffusion tensor imaging helps identify shunt-responsive normal pressure hydrocephalus patients among probable iNPH cohort

Authors: Vojtěch Sedlák, Adéla Bubeníková, Petr Skalický, Aleš Vlasák, Helen Whitley, David Netuka, Vladimír Beneš, Vladimír Beneš III, Ondřej Bradáč

Published in: Neurosurgical Review | Issue 1/2023

Abstract

The aim of this study was to investigate whether white matter changes as measured by diffusion tensor imaging (DTI) can help differentiate shunt-responsive idiopathic normal pressure hydrocephalus (iNPH) patients from patients with other causes of gait disturbances and/or cognitive decline with ventriculomegaly whose clinical symptoms do not improve significantly after cerebrospinal fluid derivation (non-iNPH). Between 2017 and 2022, 85 patients with probable iNPH underwent prospective preoperative magnetic resonance imaging (MRI) and comprehensive clinical workup. Patients with clinical symptoms of iNPH, positive result on lumbar infusion test, and gait improvement after 120-h lumbar drainage were diagnosed with iNPH and underwent shunt-placement surgery. Fractional anisotropy (FA) and mean diffusivity (MD) values for individual regions of interest were extracted from preoperative MRI, using the TBSS pipeline of FSL toolkit. These FA and MD values were then compared to results of clinical workup and established diagnosis of iNPH. An identical MRI protocol was performed on 13 age- and sex-matched healthy volunteers. Statistically significant differences in FA values of several white matter structures were found not only between iNPH patients and healthy controls but also between iNPH and non-iNPH patients. ROI that showed best diagnostic ability when differentiating iNPH among probable iNPH cohort was uncinate fasciculus, with AUC of 0.74 (p < 0.001). DTI methods of white matter analysis using standardised methods of ROI extraction can help in differentiation of iNPH patients not only from healthy patients but also from patients with other causes of gait disturbances with cognitive decline and ventriculomegaly.

Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM (2005) Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery. 57(3 Suppl):S4–16; discussion ii-v. https://doi.org/10.1227/01.neu.0000168185.29659.c5

Martín-Láez R, Caballero-Arzapalo H, López-Menéndez LÁ, Arango-Lasprilla JC, Vázquez-Barquero A (2015) Epidemiology of idiopathic normal pressure hydrocephalus: a systematic review of the literature. World Neurosurg 84(6):2002–2009. https://doi.org/10.1016/j.wneu.2015.07.005CrossRefPubMed

Jaraj D et al (2014) Prevalence of idiopathic normal-pressure hydrocephalus. Neurology 82(16):1449–1454. https://doi.org/10.1212/wnl.0000000000000342CrossRefPubMedPubMedCentral

Popal AM, Zhu Z, Guo X et al (2021) Outcomes of ventriculoperitoneal shunt in patients with idiopathic normal-pressure hydrocephalus 2 years after surgery. Front Surg. 8:641561. https://doi.org/10.3389/fsurg.2021.641561CrossRefPubMedPubMedCentral

Peterson KA, Savulich G, Jackson D, Killikelly C, Pickard JD, Sahakian BJ (2016) The effect of shunt surgery on neuropsychological performance in normal pressure hydrocephalus: a systematic review and meta-analysis. J Neurol 263(8):1669–1677. https://doi.org/10.1007/s00415-016-8097-0CrossRefPubMedPubMedCentral

McGirt MJ, Woodworth G, Coon AL, Thomas G, Williams MA, Rigamonti D (2005) Diagnosis, treatment, and analysis of long-term outcomes in idiopathic normal-pressure hydrocephalus. Neurosurgery. 57(4):699–705; discussion 699–705. https://doi.org/10.1093/neurosurgery/57.4.699

Andrén K, Wikkelsø C, Hellström P, Tullberg M, Jaraj D (2021) Early shunt surgery improves survival in idiopathic normal pressure hydrocephalus. Eur J Neurol 28(4):1153–1159. https://doi.org/10.1111/ene.14671CrossRefPubMedPubMedCentral

Tullberg M, Persson J, Petersen J, Hellström P, Wikkelsø C, Lundgren-Nilsson Å (2018) Shunt surgery in idiopathic normal pressure hydrocephalus is cost-effective—a cost utility analysis. Acta Neurochir (Wien) 160(3):509–518. https://doi.org/10.1007/s00701-017-3394-7CrossRefPubMed

Virhammar J, Laurell K, Cesarini KG, Larsson EM (2014) Preoperative prognostic value of MRI findings in 108 patients with idiopathic normal pressure hydrocephalus. AJNR Am J Neuroradiol 35(12):2311–2318. https://doi.org/10.3174/ajnr.A4046CrossRefPubMedPubMedCentral

10.

Vlasák A, Gerla V, Skalický P et al (2022) Boosting phase-contrast MRI performance in idiopathic normal pressure hydrocephalus diagnostics by means of machine learning approach. Neurosurg Focus 52(4):E6. https://doi.org/10.3171/2022.1.FOCUS21733CrossRefPubMed

11.

Kockum K et al (2020) Diagnostic accuracy of the INPH Radscale in idiopathic normal pressure hydrocephalus. PloS One 15(4):e0232275. https://doi.org/10.1371/journal.pone.0232275CrossRefPubMedPubMedCentral

12.

Carlsen JF et al (2022) Can shunt response in patients with idiopathic normal pressure hydrocephalus be predicted from preoperative brain imaging? A retrospective study of the diagnostic use of the Normal Pressure Hydrocephalus Radscale in 119 Patients. AJNR Am J Neuroradiol 43(2):223–229. https://doi.org/10.3174/ajnr.A7378CrossRefPubMedPubMedCentral

13.

Laticevschi T, Lingenberg A, Armand S, Griffa A, Assal F, Allali G (2021) Can the radiological scale “iNPH Radscale” predict tap test response in idiopathic normal pressure hydrocephalus? J Neurol Sci. 420(117239):117239. https://doi.org/10.1016/j.jns.2020.117239CrossRefPubMed

14.

Carlsen JF, Backlund ADL, Mardal CA et al (2022) Can shunt response in patients with idiopathic normal pressure hydrocephalus be predicted from preoperative brain imaging? A retrospective study of the diagnostic use of the Normal Pressure Hydrocephalus Radscale in 119 patients. AJNR Am J Neuroradiol 43(2):223–229. https://doi.org/10.3174/ajnr.A7378CrossRefPubMedPubMedCentral

15.

Basser PJ, Mattiello J, Lebihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103(3):247–254. https://doi.org/10.1006/jmrb.1994.1037CrossRefPubMed

16.

O’Donnell LJ, Westin CF (2011) An introduction to diffusion tensor image analysis. Neurosurg Clin N Am. 22(2):185-196 viii. https://doi.org/10.1016/j.nec.2010.12.004CrossRefPubMedPubMedCentral

17.

Grazzini I, Venezia D, Cuneo GL (2021) The role of diffusion tensor imaging in idiopathic normal pressure hydrocephalus: a literature review. Neuroradiol J 34(2):55–69. https://doi.org/10.1177/1971400920975153CrossRefPubMed

18.

Koyama T, Marumoto K, Domen K, Miyake H (2013) White matter characteristics of idiopathic normal pressure hydrocephalus: a diffusion tensor tract-based spatial statistic study. Neurol Med Chir (Tokyo) 53(9):601–608. https://doi.org/10.2176/nmc.oa2012-0307CrossRefPubMed

19.

Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219. https://doi.org/10.1016/j.neuroimage.2004.07.051CrossRefPubMed

20.

Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL Neuroimage 62(2):782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015CrossRefPubMed

21.

Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31(4):1487–1505. https://doi.org/10.1016/j.neuroimage.2006.02.024CrossRefPubMed

22.

Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17(3):143–155. https://doi.org/10.1002/hbm.10062CrossRefPubMedPubMedCentral

23.

J.L.R. Andersson, M. Jenkinson and S. Smith. Non-linear optimisation. FMRIB technical report TR07JA1. www.fmrib.ox.ac.uk/analysis/techrep. Accessed 7 May 2023

24.

J.L.R. Andersson, M. Jenkinson and S. Smith. Non-linear registration, aka spatial normalisation FMRIB technical report TR07JA2. www.fmrib.ox.ac.uk/analysis/techrep. Accessed 7 May 2023

25.

Rueckert D, Sonoda LI, Hayes C, Hill DL, Leach MO, Hawkes DJ (1999) Nonrigid registration using free-form deformations: application to breast MR images. IEEE Trans Med Imaging 18(8):712–721. https://doi.org/10.1109/42.796284CrossRefPubMed

26.

Mori et al (2005) MRI atlas of human white matter. Elsevier, Amsterdam, The Netherlands

27.

Nakanishi A, Fukunaga I, Hori M et al (2013) Microstructural changes of the corticospinal tract in idiopathic normal pressure hydrocephalus: a comparison of diffusion tensor and diffusional kurtosis imaging. Neuroradiology 55(8):971–976. https://doi.org/10.1007/s00234-013-1201-6CrossRefPubMed

28.

Metoki A, Alm KH, Wang Y, Ngo CT, Olson IR (2017) Never forget a name: white matter connectivity predicts person memory. Brain Struct Funct 222(9):4187–4201. https://doi.org/10.1007/s00429-017-1458-3CrossRefPubMedPubMedCentral

29.

Carter CS, Botvinick MM, Cohen JD (1999) The contribution of the anterior cingulate cortex to executive processes in cognition. Rev Neurosci 10(1):49–57. https://doi.org/10.1515/revneuro.1999.10.1.49CrossRefPubMed

30.

Saito M, Nishio Y, Kanno S et al (2011) Cognitive profile of idiopathic normal pressure hydrocephalus. Dement Geriatr Cogn Dis Extra 1(1):202–211. https://doi.org/10.1159/000328924CrossRefPubMedPubMedCentral

31.

Wang Y, Metoki A, Smith DV et al (2020) Multimodal mapping of the face connectome. Nat Hum Behav 4(4):397–411. https://doi.org/10.1038/s41562-019-0811-3CrossRefPubMedPubMedCentral

32.

Kang K, Hwang SK, Lee HW (2013) Shunt-responsive idiopathic normal pressure hydrocephalus patient with delayed improvement after tap test. J Korean Neurosurg Soc 54(5):437–440. https://doi.org/10.3340/jkns.2013.54.5.437CrossRefPubMedPubMedCentral

Title: Diffusion tensor imaging helps identify shunt-responsive normal pressure hydrocephalus patients among probable iNPH cohort
Authors: Vojtěch Sedlák
Adéla Bubeníková
Petr Skalický
Aleš Vlasák
Helen Whitley
David Netuka
Vladimír Beneš
Vladimír Beneš III
Ondřej Bradáč
Publication date: 01-12-2023
Publisher: Springer Berlin Heidelberg
Keywords: Hydrocephalus
Hydrocephalus
Hydrocephalus
Magnetic Resonance Imaging
Magnetic Resonance Imaging
Published in: Neurosurgical Review / Issue 1/2023
Print ISSN: 0344-5607
Electronic ISSN: 1437-2320
DOI: https://doi.org/10.1007/s10143-023-02078-1

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Diffusion tensor imaging helps identify shunt-responsive normal pressure hydrocephalus patients among probable iNPH cohort

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