BACKGROUND: Idiopathic normal pressure hydrocephalus (iNPH) is a progressive disease characterized by disproportionate ventricular enlargement at brain imaging with gait disturbance and an increased risk of falling. Gait assessment is a key feature in the diagnosis of iNPH and characterization of post-surgical outcomes. RESEARCH QUESTION: How do gait parameters change 24 h after CSF tap test (CSFTT) and after ventriculoperitoneal shunt surgery? METHODS: The PRISMA guidelines were used to perform the systematic review. We conducted a search of the following electronic databases: PubMed, Medline, Web of Science and EBSCO. We included studies focusing on gait changes occurring 24 h after a CSFTT or after ventriculoperitoneal shunt surgery in patients with iNPH. All articles were assessed for methodological quality using an adapted version of The Standard Quality Assessment Criteria for Evaluating Primary Research Papers checklist. RESULTS: Twenty-seven studies were included in the systematic review. Studies were highly heterogeneous due to lack of standardization of CSFTT or shunt surgery methodology, with varying amounts of CSF removed during the tap test (20-50 ml) and varying time of outcome assessment after shunt surgery. Dynamic equilibrium measurements are generally used to assess preoperative levels of cardinal symptoms and postoperative outcomes in iNPH. The most sensitive spatio-temporal parameter assessed 24 h after CSFTT was self-selected walking speed followed by stride length, which increased significantly. Cadence is hence not suitable to consider in the evaluation of effect of CSFTT and shunt surgery. Changes in balance-related gait parameters after CSFTT and shunt surgery are still a controversial area of research. CONCLUSION: Gait assessment is a key feature in the diagnosis of iNPH and characterization of post-surgical outcomes. Dynamic equilibrium measurements are generally used to assess preoperative levels of cardinal symptoms and postoperative outcomes in iNPH, but quantitative and standardized gait analysis procedures are missing. Changes in balance-related gait parameters after CSFTT might be useful in deciding whether to perform shunt surgery in iNPH patients who hope for improvement in gait ability. The dual-task paradigm after CSFTT could improve the clinical evaluation of higher level frontal gait disturbances in patients with suspected iNPH before shunting.

Department of Neurology Faculty of Medicine and Dentistry Palacky University and University Hospital Olomouc Olomouc Czech Republic

Leenaards Memory Center Department of Clinical Neurosciences Lausanne University Hospital and University of Lausanne Lausanne Switzerland

Medical Image Processing Laboratory Neuro 10 Institute École Polytechnique Fédérale De Lausanne Geneva Switzerland

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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. PubMed

Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM. INPH guidelines, part II: diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005;57(3):S2-17. PubMed

Palm WM, Walchenbach R, Bruinsma B, Admiraal-Behloul F, Middelkoop HAM, Launer LJ, et al. Intracranial compartment volumes in normal pressure hydrocephalus: volumetric assessment versus outcome. AJNR Am J Neuroradiol. 2006;27(1):76–9. PubMed PMC

Davis A, Luciano M, Moghekar A, Yasar S. Assessing the predictive value of common gait measure for predicting falls in patients presenting with suspected normal pressure hydrocephalus. BMC Neurol. 2021;21(1):60. 10.1186/s12883-021-02068-0. PubMed PMC

Morel E, Armand S, Assal F, Allali G. Is frontal gait a myth in normal pressure hydrocephalus? J Neurol Sci. 2019;402:175–9. PubMed

Fisher CM. The clinical picture in occult hydrocephalus. Neurosurgery. 1977;24:270–84. PubMed

Ferrari A, Milletti D, Palumbo P, Giannini G, Cevoli S, Magelli E, Albini-Riccioli L, Mantovani P, Cortelli P, Chiari L, Palandri G. Gait apraxia evaluation in normal pressure hydrocephalus using inertial sensors. Clinical correlates, ventriculoperitoneal shunt outcomes, and tap-test predictive capacity. Fluid Barrier CNS. 2022;19(1):51. 10.1186/s12987-022-00350-y. PubMed PMC

Agostini V, Lanotte M, Carlone M, Campagnoli M, Azzolin I, Scarafia R, et al. Instrumented gait analysis for an objective pre-/postassessment of tap test in normal pressure hydrocephalus. Arch Phys Med Rehabil. 2015;96(7):1235–41. 10.1016/j.apmr.2015.02.014. PubMed

Hausdorff JM. Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos Interdiscipl J Nonlinear Sci. 2009;19:026113. 10.1063/1.3147408. PubMed PMC

Nikaido Y, Urakami H, Akisue T, Okada Y, Katsuta N, Kawami Y, et al. Associations among falls, gait variability, and balance function in idiopathic normal pressure hydrocephalus. Clin Neurol Neurosurg. 2019;183: 105385. 10.1016/j.clineuro.2019.105385. PubMed

Knutsson E, Lying-Tunell U. Gait apraxia in normal-pressure hydrocephalus: patterns of movement and muscle activation. Neurology. 1985;35(2):155–60. 10.1212/wnl.35.2.155. PubMed

Halperin JJ, Kurlan R, Schwalb JM, Cusimano MD, Gronseth G, Gloss D. Practice guideline: Idiopathic normal pressure hydrocephalus: response to shunting and predictors of response: report of the guideline development, dissemination, and implementation subcommittee of the American academy of neurology. Neurology. 2015;85(23):2063–71. 10.1212/WNL.0000000000002193. PubMed PMC

J Simon, I Jusue-Torres, V Prabhu, D Anderson, M J Schneck. 2023. Chapter 12—normal pressure hydrocephalus. In: R S Tubbs, J Iwanaga, E B Rizk, A V DAntoni, AS Dumont (Eds.), Cerebrospinal fluid and subarachnoid space. Academic Press: Cambridge. Pp. 157–171.

Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021. 10.1136/BMJ.N71. PubMed PMC

Morris M, McGinley J, Huxham F, Collier J, Iansek R. Constraints on the kinetic, kinematic and spatiotemporal parameters of gait in Parkinson’s disease. Hum Mov Sci. 1999;18(2–3):461–83. 10.1016/S0167-9457(99)00020-2.

Kmet LM, Cook LS, Lee RC. Standard quality assess-ment criteria for evaluating primary research papersfrom a variety of fields. Edmont Alta Herit Age Found Med Res. 2004. 10.7939/R37M04F16.

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(9):1678–86. 10.1016/s1388-2457(00)00362-x. PubMed

Schniepp R, Trabold R, Romagna A, Akrami F, Hesselbarth K, Wuehr M, et al. Walking assessment after lumbar puncture in normal-pressure hydrocephalus: a delayed improvement over 3 days. J Neurosurg. 2017;126(1):148–57. 10.3171/2015.12.JNS151663. PubMed

Marques B, Laidet M, Armand S, Assal F, Allali G. CSF tapping also improves mental imagery of gait in normal pressure hydrocephalus. J Neural Transm (Vienna). 2017;124(11):1401–5. 10.1007/s00702-017-1766-z. PubMed

Allali G, Laidet M, Armand S, Momjian S, Marques B, Sajet A, et al. A combined cognitive and gait quantification to identify normal pressure hydrocephalus from its mimics: the Geneva’s protocol. Clin Neurol Neurosurg. 2017;160:5–11. 10.1016/j.clineuro.2017.06.001. PubMed

Bovonsunthonchai S, Witthiwej T, Ngamsombat C, Sathornsumetee S, Vachalathiti R, Muangpaisan W, et al. Effect of spinal tap test on the performance of sit-to-stand, walking, and turning in patients with idiopathic normal pressure hydrocephalus. Nagoya J Med Sci. 2018;80(1):53–60. 10.18999/nagjms.80.1.53. PubMed PMC

Souza RKM, Rocha SFBD, Martins RT, Kowacs PA, Ramina R. Gait in normal pressure hydrocephalus: characteristics and effects of the CSF tap test. Arq Neuropsiquiatr. 2018;76(5):324–31. 10.1590/0004-282X20180037. PubMed

Lim YH, Ko PW, Park KS, Hwang SK, Kim SH, Han J, et al. Quantitative gait analysis and cerebrospinal fluid tap test for idiopathic normal-pressure hydrocephalus. Sci Rep. 2019;9(1):16255. 10.1038/s41598-019-52448-3. PubMed PMC

Giannini G, Palandri G, Ferrari A, Oppi F, Milletti D, Albini-Riccioli L, Mantovani P, Magnoni S, Chiari L, Cortelli P, Cevoli S. Bologna PRO-Hydro study group. A prospective evaluation of clinical and instrumental features before and after ventriculo-peritoneal shunt in patients with idiopathic normal pressure hydrocephalus: the Bologna PRO-Hydro study. Parkinsonism Relat Disord. 2019;66:117–24. 10.1016/j.parkreldis.2019.07.021. PubMed

Isik AT, Kaya D, AtesBulut E, Dokuzlar O, Soysal P. The outcomes of serial cerebrospinal fluid removal in elderly patients with idiopathic normal pressure hydrocephalus. Clin Interv Aging. 2019;14:2063–9. 10.2147/CIA.S228257. PubMed PMC

Ferrari A, Milletti D, Giannini G, Cevoli S, Oppi F, Palandri G, et al. The effects of cerebrospinal fluid tap-test on idiopathic normal pressure hydrocephalus: an inertial sensors based assessment. J Neuroeng Rehabil. 2020;17(1):7. 10.1186/s12984-019-0638-1. PubMed PMC

Sun Y, Liang S, Yu Y, Yang Y, Lu J, Wu J, et al. Plantar pressure-based temporal analysis of gait disturbance in idiopathic normal pressure hydrocephalus: indications from a pilot longitudinal study. Comput Method Progr Biomed. 2022;217: 106691. 10.1016/j.cmpb.2022.106691. PubMed

Griffa A, Bommarito G, Assal F, Herrmann FR, Van De Ville D, Allali G. Dynamic functional networks in idiopathic normal pressure hydrocephalus: alterations and reversibility by CSF tap test. Hum Brain Mapp. 2021;42(5):1485–502. 10.1002/hbm.25308. PubMed PMC

Morel E, Armand S, Assal F, Allali G. Normal pressure hydrocephalus and CSF tap test response: the gait phenotype matters. J Neural Transm (Vienna). 2021;128(1):121–5. 10.1007/s00702-020-02270-3. PubMed PMC

Chunyan L, Rongrong H, Youping W, Hongliang L, Qiong Y, Xinget L. Gait characteristics and effects of the cerebrospinal fluid tap test in probable idiopathic normal pressure hydrocephalus. Clin Neurol Neurosurg. 2021;210: 106952. 10.1016/j.clineuro.2021.106952. PubMed

Matsuoka T, Fujimoto K, Kawahara M. Comparison of comfortable and maximum walking speed in the 10-meter walk test during the cerebrospinal fluid tap test in iNPH patients: a retrospective study. Clin Neurol Neurosurg. 2022;212: 107049. 10.1016/j.clineuro.2021.107049. PubMed

Chen CPC, Huang YC, Chang CN, Chen JL, Hsu CC, Lin WY. Changes of cerebrospinal fluid protein concentrations and gait patterns in geriatric normal pressure hydrocephalus patients after ventriculoperitoneal shunting surgery. Exp Gerontol. 2018;106:109–15. 10.1016/j.exger.2018.01.027. PubMed

Nikaido Y, Akisue T, Kajimoto Y, Ikeji T, Kawami Y, Urakami H, et al. The effect of CSF drainage on ambulatory center of mass movement in idiopathic normal pressure hydrocephalus. Gait Posture. 2018;63:5–9. 10.1016/j.gaitpost.2018.04.024. PubMed

Kitade I, Kitai R, Neishi H, Kikuta KI, Shimada S, Matsumine A. Relationship between gait parameters and MR imaging in idiopathic normal pressure hydrocephalus patients after shunt surgery. Gait Posture. 2018;61:163–8. 10.1016/j.gaitpost.2018.01.008. PubMed

Song M, Lieberman A, Fife T, Nielsen M, Hayden S, Sabbagh M, et al. A prospective study on gait dominant normal pressure hydrocephalus. Acta Neurol Scand. 2019;139(4):389–94. 10.1111/ane.13064. PubMed

Baltateanu D, Ciobanu I, Berteanu M. The effects of ventriculoperitoneal shunt on gait performance. J Med Life. 2019;12(2):194–8. 10.25122/jml-2019-1004. PubMed PMC

Sundström N, Rydja J, Virhammar J, Kollén L, Lundin F, Tullberg M, et al. The timed up and go test in idiopathic normal pressure hydrocephalus: a nationwide study of 1300 patients. Fluid Barrier CNS. 2022;19:4. 10.1186/s12987-021-00298-5. PubMed PMC

Gago MF, Ferreira F, Bicho E. Quantitative gait analysis value as a predictor of shunt surgery effectiveness in normal pressure hydrocephalus: a technical note. Clin Neurol Neurosurg. 2022;221: 107405. 10.1016/j.clineuro.2022.107405. PubMed

Hülser M, Spielmann H, Oertel J, Sippl C. Motor skills, cognitive impairment, and quality of life in normal pressure hydrocephalus: early effects of shunt placement. Acta Neurochir (Wien). 2022;164(7):1765–75. 10.1007/s00701-022-05149-2. PubMed PMC

Hallqvist C, Grönstedt H, Arvidsson L. Gait, falls, cognitive function, and health-related quality of life after shunt-treated idiopathic normal pressure hydrocephalus-a single-center study. Acta Neurochir (Wien). 2022;164(9):2367–73. 10.1007/s00701-022-05309-4. PubMed PMC

Giannini G, Jusue-Torres I, Mantovani P, Mazza L, Pirina A, Valsecchi N, et al. INPH and parkinsonism: a positive shunt response with a negative tap test. Front Neurol. 2023;14:1150258. 10.3389/fneur.2023.1150258. PubMed PMC

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

Mori E, Ishikawa M, Kato T, Kazui H, Miyake H, Miyajima M, Nakajima M, Hashimoto M, Kuriyama N, Tokuda T, Ishii K, Kaijima M, Hirata Y, Saito M, Arai H. Japanese society of normal pressure hydrocephalus. Guidelines for management of idiopathic normal pressure hydrocephalus: second edition. Neurol Med Chir (Tokyo). 2012;52(11):775–809. 10.2176/nmc.52.775. PubMed

Marmarou A, Young HF, Aygok GA, Sawauchi S, Tsuji O, Yamamoto T, Dunbar J. Diagnosis and management of idiopathic normal-pressure hydrocephalus: a prospective study in 151 patients. J Neurosurg. 2005;102(6):987–97. 10.3171/jns.2005.102.6.0987. PubMed

Stolze 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(3):289–97. 10.1136/jnnp.70.3.289. PubMed PMC

Mori L, Collino F, Marzi A, Pellegrino L, Ponzano M, Chiaroet D, et al. Useful outcome measures in INPH patients evaluation. Front Neurol. 2023;14:1201932. 10.3389/fneur.2023.1201932. PubMed PMC

Nikaido Y, Urakami H, Okada Y, Kajimoto Y, Ishida N, Kawami Y, et al. Dynamic gait stability in patients with idiopathic normal pressure hydrocephalus with high and low fall-risk. Clin Biomech (Bristol, Avon). 2022;99: 105757. 10.1016/j.clinbiomech.2022.105757. PubMed

Ishikawa M, Hashimoto M, Mori E, Kuwana N, Kazui H. The value of the cerebrospinal fluid tap test for predicting shunt effectiveness in idiopathic normal pressure hydrocephalus. Fluid Barrier CNS. 2012;9(1):1. 10.1186/2045-8118-9-1. PubMed PMC

Thavarajasingam SG, El-Khatib M, Rea M, Russo S, Lemcke J, Al-Nusair L, Vajkoczy P. Clinical predictors of shunt response in the diagnosis and treatment of idiopathic normal pressure hydrocephalus: a systematic review and meta-analysis. Acta Neurochir (Wien). 2021;163(10):2641–72. 10.1007/s00701-021-04922-z. PubMed PMC

McGirt MJ, Woodworth G, Coon AL, Thomas G, Williams MA, Rigamonti D. Diagnosis, treatment, and analysis of longterm outcomes in idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005;57(4):699–705. PubMed

Allali G, Laidet M, Beauchet O, Herrmann FR, Assal F, Armand S. Dual-task related gait changes after CSF tapping: a new way to identify idiopathic normal pressure hydrocephalus. J Neuroeng Rehabil. 2013;10:117. 10.1186/1743-0003-10-117. PubMed PMC

Lilja-Lund O, Nyberg L, Maripuu M, Laurell K. Dual-task performance in older adults with and without idiopathic normal pressure hydrocephalus. Front Aging Neurosci. 2022;30(14): 904194. 10.3389/fnagi.2022.904194. PubMed PMC

Laidet M, Herrmann FR, Momjian S, Assal F, Allali G. Improvement in executive subfunctions following cerebrospinal fluid tap test identifies idiopathic normal pressure hydrocephalus from its mimics. Eur J Neurol. 2015;22(12):1533–9. 10.1111/ene.12779. PubMed

Möhwald K, Wuehr M, Decker J, Asch EM, Schenkel F, Illigens B, Schniepp R. Quantification of pathological gait parameter thresholds of idiopathic normal pressure hydrocephalus patients in clinical gait analysis. Sci Rep. 2022;12(1):18295. 10.1038/s41598-022-22692-1. PubMed PMC

Ryo O, Yasuaki I, Yoshiaki O, Takatoshi S. The necessity of gait evaluation on the 7th day after tap tests for the idiopathic normal pressure hydrocephalus patients. BMC Geriatr. 2023;23(1):776. 10.1186/s12877-023-04481-1. PubMed PMC