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Published in: Fluids and Barriers of the CNS 1/2022

Open Access 01-12-2022 | Hydrocephalus | Research

Gait apraxia evaluation in normal pressure hydrocephalus using inertial sensors. Clinical correlates, ventriculoperitoneal shunt outcomes, and tap-test predictive capacity

Authors: Alberto Ferrari, David Milletti, Pierpaolo Palumbo, Giulia Giannini, Sabina Cevoli, Elena Magelli, Luca Albini-Riccioli, Paolo Mantovani, Pietro Cortelli, Lorenzo Chiari, Giorgio Palandri

Published in: Fluids and Barriers of the CNS | Issue 1/2022

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Abstract

Background

Idiopathic normal pressure hydrocephalus (iNPH) is a neurological condition with gait apraxia signs from its early manifestation. Ventriculoperitoneal shunt (VPS) is a surgical procedure available for treatment. The Cerebrospinal fluid Tap Test (CSF-TT) is a quick test used as selection criterion for VPS treatment. Its predictive capacity for VPS outcomes is still sub judice. This study is aimed to test the hypothesis that wearable motion sensors provide valid measures to manage iNPH patients with gait apraxia.

Methods

Forty-two participants of the Bologna PRO-Hydro observational cohort study were included in the analyses. The participants performed the Timed Up and Go (TUG) and the 18 m walking test (18mW) with inertial sensors at baseline, three days after the CSF-TT, and six months after VPS. 21 instrumental variables described gait and postural transitions from TUG and 18mW recordings. Furthermore, participants were clinically assessed with scales (clinical variables). We tested the hypothesis by analysing the concurrent validity of instrumental and clinical variables, their individual- and group-level responsiveness to VPS, and their predictive validity for VPS outcomes after CSF-TT.

Results

The instrumental variables showed moderate to high correlation with the clinical variables. After VPS, most clinical and instrumental variables showed statistically significant improvements that reflect a reduction of apraxic features of gait. Most instrumental variables, but only one clinical variable (i.e., Tinetti POMA), had predictive value for VPS outcomes (significant adjusted R2 in the range 0.12–0.70).

Conclusions

These results confirm that wearable inertial sensors may represent a valid tool to complement clinical evaluation for iNPH assessment and prognosis.
Appendix
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Literature
1.
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.CrossRef 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.CrossRef
2.
go back to reference 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.CrossRef 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.CrossRef
3.
go back to reference Morel E, Armand S, Assal F, Allali G. Is frontal gait a myth in normal pressure hydrocephalus? J Neurol Sci. 2019;402:175–9.CrossRef Morel E, Armand S, Assal F, Allali G. Is frontal gait a myth in normal pressure hydrocephalus? J Neurol Sci. 2019;402:175–9.CrossRef
4.
go back to reference Dale ML, Curtze C, Nutt JG. Apraxia of gait- or apraxia of postural transitions? Parkinsonism Relat Disord. 2018;50:19–22.CrossRef Dale ML, Curtze C, Nutt JG. Apraxia of gait- or apraxia of postural transitions? Parkinsonism Relat Disord. 2018;50:19–22.CrossRef
5.
go back to reference Fisher CM. The clinical picture in occult hydrocephalus. Neurosurgery. 1977;24:270–84.CrossRef Fisher CM. The clinical picture in occult hydrocephalus. Neurosurgery. 1977;24:270–84.CrossRef
6.
go back to reference Meyer JS, Barron DW. Apraxia of gait: a clinico-physiological study. Brain. 1960;83:261–84.CrossRef Meyer JS, Barron DW. Apraxia of gait: a clinico-physiological study. Brain. 1960;83:261–84.CrossRef
7.
go back to reference Toma AK, Papadopoulos MC, Stapleton S, Kitchen ND, Watkins LD. Systematic review of the outcome of shunt surgery in idiopathic normal-pressure hydrocephalus. Acta Neurochir (Wien). 2013;155:1977–80.CrossRef Toma AK, Papadopoulos MC, Stapleton S, Kitchen ND, Watkins LD. Systematic review of the outcome of shunt surgery in idiopathic normal-pressure hydrocephalus. Acta Neurochir (Wien). 2013;155:1977–80.CrossRef
8.
go back to reference 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 AAN Enterprises. 2015;85:2063–71. 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 AAN Enterprises. 2015;85:2063–71.
9.
go back to reference Scully AE, Lim ECW, Teow PP, Tan DML. A systematic review of the diagnostic utility of simple tests of change after trial removal of cerebrospinal fluid in adults with normal pressure hydrocephalus. Clin Rehabil. 2018;32:942–53.CrossRef Scully AE, Lim ECW, Teow PP, Tan DML. A systematic review of the diagnostic utility of simple tests of change after trial removal of cerebrospinal fluid in adults with normal pressure hydrocephalus. Clin Rehabil. 2018;32:942–53.CrossRef
10.
go back to reference Virhammar J, Cesarini KG, Laurell K. The CSF tap test in normal pressure hydrocephalus: evaluation time, reliability and the influence of pain. Eur J Neurol. 2012;19:271–6.CrossRef Virhammar J, Cesarini KG, Laurell K. The CSF tap test in normal pressure hydrocephalus: evaluation time, reliability and the influence of pain. Eur J Neurol. 2012;19:271–6.CrossRef
11.
go back to reference Gallagher R, Marquez J, Osmotherly P. Gait and balance measures can identify change from a cerebrospinal fluid tap test in idiopathic normal pressure hydrocephalus. Arch Phys Med Rehabil. 2018;99:2244–50.CrossRef Gallagher R, Marquez J, Osmotherly P. Gait and balance measures can identify change from a cerebrospinal fluid tap test in idiopathic normal pressure hydrocephalus. Arch Phys Med Rehabil. 2018;99:2244–50.CrossRef
12.
go back to reference Marmarou A, Bergsneider M, Klinge P, Relkin N, Black PM. The value of supplemental prognostic tests for the preoperative assessment of idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005;57:S17-28.PubMed Marmarou A, Bergsneider M, Klinge P, Relkin N, Black PM. The value of supplemental prognostic tests for the preoperative assessment of idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005;57:S17-28.PubMed
13.
go back to reference Mihalj M, Dolić K, Kolić K, Ledenko V. CSF tap test - Obsolete or appropriate test for predicting shunt responsiveness? A systemic review. J Neurol Sci. 2016;362:78–84.CrossRef Mihalj M, Dolić K, Kolić K, Ledenko V. CSF tap test - Obsolete or appropriate test for predicting shunt responsiveness? A systemic review. J Neurol Sci. 2016;362:78–84.CrossRef
14.
go back to reference Gor-García-Fogeda MD, Cano de la Cuerda R, Carratalá Tejada M, Alguacil-Diego IM, Molina-Rueda F. Observational gait assessments in people with neurological disorders: a systematic review. Arch Phys Med Rehabil. 2016;97:131–40. Gor-García-Fogeda MD, Cano de la Cuerda R, Carratalá Tejada M, Alguacil-Diego IM, Molina-Rueda F. Observational gait assessments in people with neurological disorders: a systematic review. Arch Phys Med Rehabil. 2016;97:131–40.
15.
go back to reference 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;96:1235–41.CrossRef 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;96:1235–41.CrossRef
16.
go back to reference Giannini G, Palandri G, Ferrari A, Oppi F, Milletti D, Albini-Riccioli L, et al. 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.CrossRef Giannini G, Palandri G, Ferrari A, Oppi F, Milletti D, Albini-Riccioli L, et al. 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.CrossRef
17.
go back to reference 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;17:7.CrossRef 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;17:7.CrossRef
18.
go back to reference Wolfsegger T, Hauser A, Wimmer S, Neuwirth K, Assar H, Topakian R. A comprehensive clinico-radiological, neuropsychological and biomechanical analysis approach to patients with idiopathic normal pressure hydrocephalus. Clin Neurol Neurosurg. 2021;201:106402.CrossRef Wolfsegger T, Hauser A, Wimmer S, Neuwirth K, Assar H, Topakian R. A comprehensive clinico-radiological, neuropsychological and biomechanical analysis approach to patients with idiopathic normal pressure hydrocephalus. Clin Neurol Neurosurg. 2021;201:106402.CrossRef
19.
go back to reference Muro-de-la-Herran A, García-Zapirain B, Méndez-Zorrilla A. Gait analysis methods: an overview of wearable and non-wearable systems, highlighting clinical applications. Sensors (Switzerland). 2014;14:3362–94.CrossRef Muro-de-la-Herran A, García-Zapirain B, Méndez-Zorrilla A. Gait analysis methods: an overview of wearable and non-wearable systems, highlighting clinical applications. Sensors (Switzerland). 2014;14:3362–94.CrossRef
20.
go back to reference Ferrari A, Ginis P, Hardegger M, Casamassima F, Rocchi L, Chiari L. A mobile kalman-filter based solution for the real-time estimation of spatio-temporal gait parameters. IEEE Trans Neural Syst Rehabil Eng. 2016;24:764–73.CrossRef Ferrari A, Ginis P, Hardegger M, Casamassima F, Rocchi L, Chiari L. A mobile kalman-filter based solution for the real-time estimation of spatio-temporal gait parameters. IEEE Trans Neural Syst Rehabil Eng. 2016;24:764–73.CrossRef
21.
go back to reference He M, Qi Z, Shao Y, Yao H, Zhang X, Zhang Y, et al. Quantitative evaluation of gait changes using APDM inertial sensors after the external lumbar drain in patients with idiopathic normal pressure hydrocephalus. Front Neurol. 2021;12: 635044.CrossRef He M, Qi Z, Shao Y, Yao H, Zhang X, Zhang Y, et al. Quantitative evaluation of gait changes using APDM inertial sensors after the external lumbar drain in patients with idiopathic normal pressure hydrocephalus. Front Neurol. 2021;12: 635044.CrossRef
22.
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.CrossRef 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.CrossRef
23.
go back to reference Allali G, Laidet M, Armand S, Momjian S, Marques B, Saj 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.CrossRef Allali G, Laidet M, Armand S, Momjian S, Marques B, Saj 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.CrossRef
24.
go back to reference Colella F, Speciali D, Bernal M, de Godoy W, Politti F, Lucareli PRG. Are we supererestimating gait assessments of patients with idiopathic normal-pressure hydrocephalus? Gait Posture England. 2019;72:12–5.CrossRef Colella F, Speciali D, Bernal M, de Godoy W, Politti F, Lucareli PRG. Are we supererestimating gait assessments of patients with idiopathic normal-pressure hydrocephalus? Gait Posture England. 2019;72:12–5.CrossRef
25.
go back to reference 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;80:53–60.PubMedPubMedCentral 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;80:53–60.PubMedPubMedCentral
26.
go back to reference Williams MA, Thomas G, de Lateur B, Imteyaz H, Rose JG, Shore WS, et al. Objective assessment of gait in normal-pressure hydrocephalus. Am J Phys Med Rehabil. 2008;87:39–45.CrossRef Williams MA, Thomas G, de Lateur B, Imteyaz H, Rose JG, Shore WS, et al. Objective assessment of gait in normal-pressure hydrocephalus. Am J Phys Med Rehabil. 2008;87:39–45.CrossRef
27.
go back to reference Lim Y-H, Ko P-W, Park K-S, Hwang SK, Kim S-H, Han J, et al. Quantitative gait analysis and cerebrospinal fluid tap test for idiopathic normal-pressure hydrocephalus. Sci Rep. 2019;9:16255.CrossRef Lim Y-H, Ko P-W, Park K-S, Hwang SK, Kim S-H, Han J, et al. Quantitative gait analysis and cerebrospinal fluid tap test for idiopathic normal-pressure hydrocephalus. Sci Rep. 2019;9:16255.CrossRef
29.
go back to reference Tinetti ME. Performance-oriented assessment of mobility problems in elderly patients. J Am Geriatr Soc. 1986;34:119–26.CrossRef Tinetti ME. Performance-oriented assessment of mobility problems in elderly patients. J Am Geriatr Soc. 1986;34:119–26.CrossRef
30.
go back to reference Kubo Y, Kazui H, Yoshida T, Kito Y, Kimura N, Tokunaga H, et al. Validation of grading scale for evaluating symptoms of idiopathic normal-pressure hydrocephalus. Dement Geriatr Cogn Disord. 2007;25:37–45.CrossRef Kubo Y, Kazui H, Yoshida T, Kito Y, Kimura N, Tokunaga H, et al. Validation of grading scale for evaluating symptoms of idiopathic normal-pressure hydrocephalus. Dement Geriatr Cogn Disord. 2007;25:37–45.CrossRef
31.
go back to reference Kahlon B, Sundbärg G, Rehncrona S. Comparison between the lumbar infusion and CSF tap tests to predict outcome after shunt surgery in suspected normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry. 2002;73:721–6.CrossRef Kahlon B, Sundbärg G, Rehncrona S. Comparison between the lumbar infusion and CSF tap tests to predict outcome after shunt surgery in suspected normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry. 2002;73:721–6.CrossRef
32.
go back to reference Linacre JM, Heinemann AW, Wright BD, Granger CV, Hamilton BB. The structure and stability of the Functional Independence Measure. Arch Phys Med Rehabil. 1994;75:127–32.CrossRef Linacre JM, Heinemann AW, Wright BD, Granger CV, Hamilton BB. The structure and stability of the Functional Independence Measure. Arch Phys Med Rehabil. 1994;75:127–32.CrossRef
33.
go back to reference Broderick JP, Adeoye O, Elm J. Evolution of the modified rankin scale and its use in future stroke trials. Stroke. 2017;48:2007–12.CrossRef Broderick JP, Adeoye O, Elm J. Evolution of the modified rankin scale and its use in future stroke trials. Stroke. 2017;48:2007–12.CrossRef
34.
go back to reference Casamassima F, Ferrari A, Milosevic B, Ginis P, Farella E, Rocchi L. A wearable system for gait training in subjects with parkinson’s disease. Sensors (Basel). 2014;14:6229–46.CrossRef Casamassima F, Ferrari A, Milosevic B, Ginis P, Farella E, Rocchi L. A wearable system for gait training in subjects with parkinson’s disease. Sensors (Basel). 2014;14:6229–46.CrossRef
35.
go back to reference Terwee C, Dekker F, Bossuyt P. A taxonomy for responsiveness? J Clin Epidemiol. 2002;55:1156.CrossRef Terwee C, Dekker F, Bossuyt P. A taxonomy for responsiveness? J Clin Epidemiol. 2002;55:1156.CrossRef
36.
go back to reference Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86:420–8.CrossRef Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86:420–8.CrossRef
37.
go back to reference Weir JP. Quantifying test-retest reliability using the intraclass correlation coefficient and the SEM. J Strength Cond Res. 2005;19:231.PubMed Weir JP. Quantifying test-retest reliability using the intraclass correlation coefficient and the SEM. J Strength Cond Res. 2005;19:231.PubMed
39.
go back to reference Cook NR. Quantifying the added value of new biomarkers: how and how not. Diagnostic Progn Res. 2018;2:14.CrossRef Cook NR. Quantifying the added value of new biomarkers: how and how not. Diagnostic Progn Res. 2018;2:14.CrossRef
40.
go back to reference Hulbert S, Ashburn A, Robert L, Verheyden G. A narrative review of turning deficits in people with Parkinson’s disease. Disabil Rehabil. 2015;37:1382–9.CrossRef Hulbert S, Ashburn A, Robert L, Verheyden G. A narrative review of turning deficits in people with Parkinson’s disease. Disabil Rehabil. 2015;37:1382–9.CrossRef
41.
go back to reference Faber MJ, Bosscher RJ, van Wieringen PCW. Clinimetric properties of the performance-oriented mobility assessment. Phys Ther. 2006;86:944–54.CrossRef Faber MJ, Bosscher RJ, van Wieringen PCW. Clinimetric properties of the performance-oriented mobility assessment. Phys Ther. 2006;86:944–54.CrossRef
42.
go back to reference Mariani B, Rochat S, Büla CJ, Aminian K. Heel and toe clearance estimation for gait analysis using wireless inertial sensors. IEEE Trans Biomed Eng. 2012;59:3162–8.CrossRef Mariani B, Rochat S, Büla CJ, Aminian K. Heel and toe clearance estimation for gait analysis using wireless inertial sensors. IEEE Trans Biomed Eng. 2012;59:3162–8.CrossRef
43.
go back to reference Plotnik M, Giladi N, Hausdorff JM. A new measure for quantifying the bilateral coordination of human gait: effects of aging and Parkinson’s disease. Exp Brain Res. 2007;181:561–70.CrossRef Plotnik M, Giladi N, Hausdorff JM. A new measure for quantifying the bilateral coordination of human gait: effects of aging and Parkinson’s disease. Exp Brain Res. 2007;181:561–70.CrossRef
Metadata
Title
Gait apraxia evaluation in normal pressure hydrocephalus using inertial sensors. Clinical correlates, ventriculoperitoneal shunt outcomes, and tap-test predictive capacity
Authors
Alberto Ferrari
David Milletti
Pierpaolo Palumbo
Giulia Giannini
Sabina Cevoli
Elena Magelli
Luca Albini-Riccioli
Paolo Mantovani
Pietro Cortelli
Lorenzo Chiari
Giorgio Palandri
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Fluids and Barriers of the CNS / Issue 1/2022
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/s12987-022-00350-y

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