CSF tap test in idiopathic normal pressure hydrocephalus: still a necessary prognostic test?
CSF tap test
Idiopathic normal pressure hydrocephalus
Multimodal MRI
Prediction
Reversible dementia
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
Sep 2022
Sep 2022
Historique:
received:
09
02
2022
accepted:
01
05
2022
revised:
29
04
2022
pubmed:
23
5
2022
medline:
12
8
2022
entrez:
22
5
2022
Statut:
ppublish
Résumé
To assess whether gait, neuropsychological, and multimodal MRI parameters predict short-term symptom reversal after cerebrospinal fluid (CSF) tap test in idiopathic normal pressure hydrocephalus (iNPH). Thirty patients (79.3 ± 5.9 years, 12 women) with a diagnosis of probable iNPH and 46 healthy controls (74.7 ± 5.4 years, 35 women) underwent comprehensive neuropsychological, quantitative gait, and multimodal MRI assessments of brain morphology, periventricular white-matter microstructure, cortical and subcortical blood perfusion, default mode network function, and white-matter lesion load. Responders were defined as an improvement of at least 10% in walking speed or timed up and go test 24 h after tap test. Univariate and multivariable tap test outcome prediction models were evaluated with logistic regression and linear support vector machine classification. Sixteen patients (53%) respondedpositively to tap test. None of the gait, neuropsychological, or neuroimaging parameters considered separately predicted outcome. A multivariable classifier achieved modest out-of-sample outcome prediction accuracy of 70% (p = .028); gait parameters, white-matter lesion load and periventricular microstructure were the main contributors. Our negative findings show that short-term symptom reversal after tap test cannot be predicted from single gait, neuropsychological, or MRI parameters, thus supporting the use of tap test as prognostic procedure. However, multivariable approaches integrating non-invasive multimodal data are informative of outcome and may be included in patient-screening procedures. Their value in predicting shunting outcome should be further explored, particularly in relation to gait and white-matter parameters.
Identifiants
pubmed: 35598251
doi: 10.1007/s00415-022-11168-x
pii: 10.1007/s00415-022-11168-x
pmc: PMC9363476
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5114-5126Subventions
Organisme : Hôpitaux Universitaires de Genève
ID : PRD-8-2019-II
Organisme : Swiss National Science Foundation
ID : 320030_173153
Pays : Switzerland
Informations de copyright
© 2022. The Author(s).
Références
Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM (2005) Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery 57:S2-4-S2-16. https://doi.org/10.1227/01.NEU.0000168185.29659.C5
doi: 10.1227/01.NEU.0000168185.29659.C5
Israelsson H, Eklund A, Malm J (2020) Cerebrospinal fluid shunting improves long-term quality of life in idiopathic normal pressure hydrocephalus. Neurosurgery 86:574–582. https://doi.org/10.1093/neuros/nyz297
doi: 10.1093/neuros/nyz297
pubmed: 31504827
Halperin JJ, Kurlan R, Schwalb JM, Cusimano MD (2015) Practice guideline: Idiopathic normal pressure hydrocephalus: Response to shunting and predictors of response. Neurology 85:2063
doi: 10.1212/WNL.0000000000002193
Macki M, Mahajan A, Shatz R, Air EL, Novikova M, Fakih M, Elmenini J, Kaur M, Bouchard KR, Funk BA, Schwalb JM (2020) Prevalence of alternative diagnoses and implications for management in idiopathic normal pressure hydrocephalus patients. Neurosurgery 87:999–1007. https://doi.org/10.1093/neuros/nyaa199
doi: 10.1093/neuros/nyaa199
pubmed: 32472677
Bergsneider M, Black PM, Klinge P, Marmarou A, Relkin N (2005) Surgical management of idiopathic normal-pressure hydrocephalus. Neurosurgery 57:S2-29-S2-39. https://doi.org/10.1227/01.NEU.0000168186.45363.4D
doi: 10.1227/01.NEU.0000168186.45363.4D
Marmarou A, Bergsneider M, Klinge P, Relkin N, Black PM (2005) The value of supplemental prognostic tests for the preoperative assessment of idiopathic normal-pressure hydrocephalus. Neurosurgery 57:S2-17-S2-28. https://doi.org/10.1227/01.NEU.0000168184.01002.60
doi: 10.1227/01.NEU.0000168184.01002.60
Acosta LMY, Stubblefield K, Conwell T, Espaillat K, Koons H, Konrad P, Fang J, Kirshner H, Davis T (2020) Protocolizing the work-up for idiopathic normal pressure hydrocephalus improves outcomes. Neurology. https://doi.org/10.1212/CPJ.0000000000001018
doi: 10.1212/CPJ.0000000000001018
pubmed: 32928974
pmcid: 7734723
Allali G, Laidet M, Armand S, Momjian S, Marques B, Saj A, Assal F (2017) A combined cognitive and gait quantification to identify normal pressure hydrocephalus from its mimics: the Geneva’s protocol. Clin Neurol Neurosurg 160:5–11. https://doi.org/10.1016/j.clineuro.2017.06.001
doi: 10.1016/j.clineuro.2017.06.001
pubmed: 28605723
Wikkelsø C, Andersson H, Blomstrand C, Lindqvist G (1982) The clinical effect of lumbar puncture in normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry 45:64–69. https://doi.org/10.1136/jnnp.45.1.64
doi: 10.1136/jnnp.45.1.64
pubmed: 7062072
pmcid: 491267
Wolfsegger T, Topakian R (2017) Cognitive impairment predicts worse short-term response to spinal tap test in normal pressure hydrocephalus. J Neurol Sci 379:222–225. https://doi.org/10.1016/j.jns.2017.06.028
doi: 10.1016/j.jns.2017.06.028
pubmed: 28716246
Allali G, Laidet M, Armand S, Saj A, Krack P, Assal F (2018) Apathy in idiopathic normal pressure hydrocephalus: a marker of reversible gait disorders. Int J Geriatr Psychiatry 33:735–742. https://doi.org/10.1002/gps.4847
doi: 10.1002/gps.4847
pubmed: 29292530
Morel E, Armand S, Assal F, Allali G (2021) Normal pressure hydrocephalus and CSF tap test response: the gait phenotype matters. J Neural Transm 128:121–125. https://doi.org/10.1007/s00702-020-02270-3
doi: 10.1007/s00702-020-02270-3
pubmed: 33106967
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. https://doi.org/10.1016/j.jns.2020.117239
doi: 10.1016/j.jns.2020.117239
pubmed: 33278661
Griffa A, Van De Ville D, Herrmann FR, Allali G (2020) Neural circuits of idiopathic normal pressure hydrocephalus: a perspective review of brain connectivity and symptoms meta-analysis. Neurosci Biobehav Rev 112:452–471. https://doi.org/10.1016/j.neubiorev.2020.02.023
doi: 10.1016/j.neubiorev.2020.02.023
pubmed: 32088348
Khoo HM, Kishima H, Tani N, Oshino S, Maruo T, Hosomi K, Yanagisawa T, Kazui H, Watanabe Y, Shimokawa T, Aso T, Kawaguchi A, Yamashita F, Saitoh Y, Yoshimine T (2016) Default mode network connectivity in patients with idiopathic normal pressure hydrocephalus. J Neurosurg 124:350–358. https://doi.org/10.3171/2015.1.JNS141633
doi: 10.3171/2015.1.JNS141633
pubmed: 26295919
Griffa A, Bommarito G, Assal F, Herrmann FR, Ville DVD, Allali G (2021) Dynamic functional networks in idiopathic normal pressure hydrocephalus: alterations and reversibility by CSF tap test. Hum Brain Mapp 42:1485–1502. https://doi.org/10.1002/hbm.25308
doi: 10.1002/hbm.25308
pubmed: 33296129
Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148. https://doi.org/10.1111/j.1532-5415.1991.tb01616.x
doi: 10.1111/j.1532-5415.1991.tb01616.x
pubmed: 1991946
Picascia M, Zangaglia R, Bernini S, Minafra B, Sinforiani E, Pacchetti C (2016) A review of cognitive impairment and differential diagnosis in idiopathic normal pressure hydrocephalus. Funct Neurol 30:217–228. https://doi.org/10.11138/FNeur/2015.30.4.217
doi: 10.11138/FNeur/2015.30.4.217
pmcid: 4758774
Cardebat D, Doyon B, Goulet P, Joanette Y (1990) Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level. Acta Neurol Belg 90:207–217
pubmed: 2124031
Drozdick LW, Wahlstrom D, Zhu J, Weiss LG (2012) The wechsler adult intelligence scale—fourth edition and the Wechsler memory scale—fourth edition. Contemporary intellectual assessment: theories, tests, and issues, 3rd edn. The Guilford Press, New York, NY, US, pp 197–223
Van der Linden M, Coyette F, Poitrenaud J, Kalafat M, Calacis F, Wyns C, Adam S (2004) L’épreuve de rappel libre/rappel indicé à 16 items (RL/RI-16). In: Van der Liden M, Adam S, Agniel A, Baisset Mouly C et al (eds) L’évaluation des troubles de la mémoire: Présentation de quatre tests de mémoire épisodique (avec leur étalonnage). Solal, Marseille
Starkstein SE, Mayberg HS, Preziosi T, Andrezejewski P, Leiguarda R, Robinson RG (1992) Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. J Neuropsychiatry Clin Neurosci 4(2):134–139
doi: 10.1176/jnp.4.2.134
Stolze H, Kuhtz-Buschbeck JP, Drücke H, Jöhnk K, Diercks C, Palmié S, Mehdorn HM, Illert M, Deuschl G (2000) Gait analysis in idiopathic normal pressure hydrocephalus—which parameters respond to the CSF tap test? Clin Neurophysiol 111:1678–1686. https://doi.org/10.1016/S1388-2457(00)00362-X
doi: 10.1016/S1388-2457(00)00362-X
pubmed: 10964082
Bommarito G, Van De Ville D, Frisoni GB, Garibotto V, Ribaldi F, Stampacchia S, Assal F, Allali G, Griffa A (2021) Alzheimer’s disease biomarkers in idiopathic normal pressure hydrocephalus: linking functional connectivity and clinical outcome. J Alzheimer’s Dis 83:1717–1728. https://doi.org/10.3233/JAD-210534
doi: 10.3233/JAD-210534
Ishikawa M, Hashimoto M, Mori E, Kuwana N, Kazui H (2012) The value of the cerebrospinal fluid tap test for predicting shunt effectiveness in idiopathic normal pressure hydrocephalus. Fluids Barriers CNS 9:1. https://doi.org/10.1186/2045-8118-9-1
doi: 10.1186/2045-8118-9-1
pubmed: 22239832
pmcid: 3293050
Kang K, Ko P-W, Jin M, Suk K, Lee H-W (2014) Idiopathic normal-pressure hydrocephalus, cerebrospinal fluid biomarkers, and the cerebrospinal fluid tap test. J Clin Neurosci 21:1398–1403. https://doi.org/10.1016/j.jocn.2013.11.039
doi: 10.1016/j.jocn.2013.11.039
pubmed: 24836892
Gunter NB, Schwarz CG, Graff-Radford J, Gunter JL, Jones DT, Graff-Radford NR, Petersen RC, Knopman DS, Jack CR (2019) Automated detection of imaging features of disproportionately enlarged subarachnoid space hydrocephalus using machine learning methods. NeuroImage Clin. 21:101605. https://doi.org/10.1016/j.nicl.2018.11.015
doi: 10.1016/j.nicl.2018.11.015
pubmed: 30497983
Kuchcinski G, Jacquiez C, Baroncini M, Machuron F, Béhal H, Dumont J, Lopes R, Delmaire C, Lebouvier T, Bottlaender M, Bordet R, Defebvre L, Pruvo J-P, Leclerc X, Hodel J (2019) Idiopathic normal-pressure hydrocephalus: diagnostic accuracy of automated sulcal morphometry in patients with ventriculomegaly. Neurosurgery 85:E747–E755. https://doi.org/10.1093/neuros/nyz121
doi: 10.1093/neuros/nyz121
pubmed: 31115469
Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, Radner H, Lechner H (1993) Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology 43:1683–1683. https://doi.org/10.1212/WNL.43.9.1683
doi: 10.1212/WNL.43.9.1683
pubmed: 8414012
Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC (2012) NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61:1000–1016. https://doi.org/10.1016/j.neuroimage.2012.03.072
doi: 10.1016/j.neuroimage.2012.03.072
pubmed: 22484410
Daducci A, Canales-Rodríguez EJ, Zhang H, Dyrby TB, Alexander DC, Thiran J-P (2015) Accelerated Microstructure Imaging via Convex Optimization (AMICO) from diffusion MRI data. Neuroimage 105:32–44. https://doi.org/10.1016/j.neuroimage.2014.10.026
doi: 10.1016/j.neuroimage.2014.10.026
pubmed: 25462697
Siasios I, Kapsalaki EZ, Fountas KN, Fotiadou A, Dorsch A, Vakharia K, Pollina J, Dimopoulos V (2016) The role of diffusion tensor imaging and fractional anisotropy in the evaluation of patients with idiopathic normal pressure hydrocephalus: a literature review. Neurosurg Focus 41:E12. https://doi.org/10.3171/2016.6.FOCUS16192
doi: 10.3171/2016.6.FOCUS16192
pubmed: 27581308
Kamiya K, Hori M, Irie R, Miyajima M, Nakajima M, Kamagata K, Tsuruta K, Saito A, Nakazawa M, Suzuki Y, Mori H, Kunimatsu A, Arai H, Aoki S, Abe O (2017) Diffusion imaging of reversible and irreversible microstructural changes within the corticospinal tract in idiopathic normal pressure hydrocephalus. NeuroImage Clin 14:663–671. https://doi.org/10.1016/j.nicl.2017.03.003
doi: 10.1016/j.nicl.2017.03.003
pubmed: 28348958
pmcid: 5358533
Virhammar J, Laurell K, Ahlgren A, Larsson E-M (2017) Arterial spin-labeling perfusion MR imaging demonstrates regional CBF decrease in idiopathic normal pressure hydrocephalus. AJNR Am J Neuroradiol 38:2081–2088. https://doi.org/10.3174/ajnr.A5347
doi: 10.3174/ajnr.A5347
pubmed: 28860216
pmcid: 7963573
Agerskov S, Hellström P, Andrén K, Kollén L, Wikkelsö C, Tullberg M (2018) The phenotype of idiopathic normal pressure hydrocephalus-a single center study of 429 patients. J Neurol Sci 391:54–60. https://doi.org/10.1016/j.jns.2018.05.022
doi: 10.1016/j.jns.2018.05.022
pubmed: 30103972
Klassen BT, Ahlskog JE (2011) Normal pressure hydrocephalus: how often does the diagnosis hold water? Neurology 77:1119–1125. https://doi.org/10.1212/WNL.0b013e31822f02f5
doi: 10.1212/WNL.0b013e31822f02f5
pubmed: 21849644
pmcid: 3265046
Nikaido Y, Urakami H, Akisue T, Okada Y, Kawami Y, Ishida N, Kuroda K, Ohno H, Kajimoto Y, Saura R (2021) Perceived and actual changes in gait balance after CSF shunting in idiopathic normal pressure hydrocephalus. Acta Neurol Scand 144:21–28. https://doi.org/10.1111/ane.13421
doi: 10.1111/ane.13421
pubmed: 33754339
Alperin N, Oliu CJ, Bagci AM, Lee SH, Kovanlikaya I, Adams D, Katzen H, Ivkovic M, Heier L, Relkin N (2014) Low-dose acetazolamide reverses periventricular white matter hyperintensities in iNPH. Neurology 82:1347–1351. https://doi.org/10.1212/WNL.0000000000000313
doi: 10.1212/WNL.0000000000000313
pubmed: 24634454
pmcid: 4001191
Ziegelitz D, Starck G, Kristiansen D, Jakobsson M, Hultenmo M, Mikkelsen IK, Hellström P, Tullberg M, Wikkelsø C (2014) Cerebral perfusion measured by dynamic susceptibility contrast MRI is reduced in patients with idiopathic normal pressure hydrocephalus. J Magn Reson Imaging 39:1533–1542. https://doi.org/10.1002/jmri.24292
doi: 10.1002/jmri.24292
pubmed: 24006249
Tuniz F, Vescovi MC, Bagatto D, Drigo D, De Colle MC, Maieron M, Skrap M (2017) The role of perfusion and diffusion MRI in the assessment of patients affected by probable idiopathic normal pressure hydrocephalus A cohort-prospective preliminary study. Fluids Barriers CNS 14:24. https://doi.org/10.1186/s12987-017-0072-3
doi: 10.1186/s12987-017-0072-3
pubmed: 28899431
pmcid: 5596479
Israelsson H, Carlberg B, Wikkelsö C, Laurell K, Kahlon B, Leijon G, Eklund A, Malm J (2017) Vascular risk factors in INPH. Neurology 88:577–585. https://doi.org/10.1212/WNL.0000000000003583
doi: 10.1212/WNL.0000000000003583
pubmed: 28062721
pmcid: 5304464
Yamada S, Ishikawa M, Miyajima M, Atsuchi M, Kimura T, Kazui H, Mori E (2017) Disease duration: the key to accurate CSF tap test in iNPH. Acta Neurol Scand 135:189–196. https://doi.org/10.1111/ane.12580
doi: 10.1111/ane.12580
pubmed: 26923727
Thavarajasingam SG, El-Khatib M, Rea M, Russo S, Lemcke J, Al-Nusair L, Vajkoczy P (2021) Clinical predictors of shunt response in the diagnosis and treatment of idiopathic normal pressure hydrocephalus: a systematic review and meta-analysis. Acta Neurochir 163:2641–2672. https://doi.org/10.1007/s00701-021-04922-z
doi: 10.1007/s00701-021-04922-z
pubmed: 34235589
Wikkelsø C, Hellström P, Klinge PM, Tans JTJ, on behalf of the E. iNPH M.S. Group (2013) 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 84:562–568. https://doi.org/10.1136/jnnp-2012-303314
doi: 10.1136/jnnp-2012-303314
pubmed: 23250963
Gallagher R, Marquez J, Osmotherly P (2019) Clinimetric properties and minimal clinically important differences for a battery of gait, balance, and cognitive examinations for the tap test in idiopathic normal pressure hydrocephalus. Neurosurgery 84:E378–E384. https://doi.org/10.1093/neuros/nyy286
doi: 10.1093/neuros/nyy286
pubmed: 30010977