Quantitative Gait Analysis and Cerebrospinal Fluid Tap Test for Idiopathic Normal-pressure Hydrocephalus

Yong-Hyun Lim, Pan-Woo Ko, Ki-Su Park, Sung Kyoo Hwang, Sung-Hee Kim, Jaehwan Han, Uicheul Yoon, Ho-Won Lee, Kyunghun Kang, Yong-Hyun Lim, Pan-Woo Ko, Ki-Su Park, Sung Kyoo Hwang, Sung-Hee Kim, Jaehwan Han, Uicheul Yoon, Ho-Won Lee, Kyunghun Kang

Abstract

We investigated gait performance utilizing a quantitative gait analysis for 2 groups: (1) idiopathic normal-pressure hydrocephalus (INPH) patients who had a positive response to the cerebrospinal fluid tap test (CSFTT) and (2) healthy controls. The aims of the study were (1) to analyze the characteristics of gait features, (2) to characterize changes in gait parameters before and after the CSFTT, and (3) to determine whether there was any relationship between stride time and stride length variability and Frontal Assessment Battery (FAB) scores in INPH patients. Twenty-three INPH patients and 17 healthy controls were included in this study. Compared with healthy controls, the gait of INPH patients was characterized by lower velocity, shorter stride length, and more broad-based gait. Patients with INPH had a longer stance phase with increased double-limb support. Variability in stride time and stride length was increased in INPH patients. Stride time and stride length variability were correlated with FAB score. After the CSFTT, gait velocity, stride length, and step width significantly improved. There were significant decreases in stride time and stride length variability. These results suggest that the CSFTT for INPH patients might improve the so-called balance-related gait parameter (ie, step width) as well. Stride time and stride length variability also responded to the CSFTT. Association between FAB scores and both stride time and stride length variability suggests involvement of similar circuits producing gait variability and frontal lobe functions in INPH patients.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Differences in CV values of stride time and stride length before and after the CSFTT for INPH patients. The mean CV values for each individual before and after the CSFTT are depicted. Filled circles show means and standard deviations.
Figure 2
Figure 2
Scatterplots illustrating the relationships between stride time and stride length variability and FAB scores at baseline for INPH patients.

References

    1. Cabral D, et al. Frequency of Alzheimer’s disease pathology at autopsy in patients with clinical normal pressure hydrocephalus. Alzheimers Dement. 2011;7:509–513. doi: 10.1016/j.jalz.2010.12.008.
    1. Kim MJ, et al. Differential diagnosis of idiopathic normal pressure hydrocephalus from other dementias using diffusion tensor imaging. AJNR. American journal of neuroradiology. 2011;32:1496–1503. doi: 10.3174/ajnr.A2531.
    1. Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH. Symptomatic occult hydrocephalus with “normal” cerebrospinal-fluid pressure: a treatable syndrome. N Engl J Med. 1965;273:117–126. doi: 10.1056/NEJM196507152730301.
    1. Owler BK, et al. Normal pressure hydrocephalus and cerebral blood flow: a PET study of baseline values. J Cereb Blood Flow Metab. 2004;24:17–23. doi: 10.1097/01.WCB.0000093326.88757.49.
    1. Wikkelsø C, Andersson H, Blomstrand C, Lindqvist G. The clinical effect of lumbar puncture in normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry. 1982;45:64–69. doi: 10.1136/jnnp.45.1.64.
    1. Ishikawa M, et al. Guidelines for management of idiopathic normal pressure hydrocephalus. Neurol Med Chir (Tokyo) 2008;48(suppl):S1–S23. doi: 10.2176/nmc.48.s1.
    1. Menz HB, Latt MD, Tiedemann A, Mun San Kwan M, Lord SR. Reliability of the GAITRite walkway system for the quantification of temporo-spatial parameters of gait in young and older people. Gait Posture. 2004;20:20–25. doi: 10.1016/s0966-6362(03)00068-7.
    1. van Uden CJ, Besser MP. Test-retest reliability of temporal and spatial gait characteristics measured with an instrumented walkway system (GAITRite) BMC Musculoskelet Disord. 2004;5:13. doi: 10.1186/1471-2474-5-13.
    1. McDonough AL, Batavia M, Chen FC, Kwon S, Ziai J. The validity and reliability of the GAITRite system’s measurements: A preliminary evaluation. Arch Phys Med Rehabil. 2001;82:419–425. doi: 10.1053/apmr.2001.19778.
    1. Nelson AJ, et al. The validity of the GaitRite and the Functional Ambulation Performance scoring system in the analysis of Parkinson gait. NeuroRehabilitation. 2002;17:255–262.
    1. Bugalho P, Guimaraes J. Gait disturbance in normal pressure hydrocephalus: a clinical study. Parkinsonism Relat Disord. 2007;13:434–437. doi: 10.1016/j.parkreldis.2006.08.007.
    1. Bugalho P, Alves L, Miguel R. Gait dysfunction in Parkinson’s disease and normal pressure hydrocephalus: a comparative study. J Neural Transm (Vienna) 2013;120:1201–1207. doi: 10.1007/s00702-013-0975-3.
    1. Stolze H, et al. Gait analysis in idiopathic normal pressure hydrocephalus–which parameters respond to the CSF tap test? Clin Neurophysiol. 2000;111:1678–1686. doi: 10.1016/s1388-2457(00)00362-x.
    1. Stolze H, et al. Comparative analysis of the gait disorder of normal pressure hydrocephalus and Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2001;70:289–297. doi: 10.1136/jnnp.70.3.289.
    1. Sasaki H, et al. Cerebral perfusion pattern of idiopathic normal pressure hydrocephalus studied by SPECT and statistical brain mapping. Ann Nucl Med. 2007;21:39–45. doi: 10.1007/bf03033998.
    1. Ishii K, et al. A multicenter brain perfusion SPECT study evaluating idiopathic normal-pressure hydrocephalus on neurological improvement. Dement Geriatr Cogn Disord. 2011;32:1–10. doi: 10.1159/000328972.
    1. Mori E. Gait disturbance in idiopathic normal pressure hydrocephalus. Brain and nerve = Shinkei kenkyu no shinpo. 2008;60:219–224.
    1. Stephenson J, et al. Gait and balance in adults with Friedreich’s ataxia. Gait Posture. 2015;41:603–607. doi: 10.1016/j.gaitpost.2015.01.002.
    1. Maki BE. Gait changes in older adults: predictors of falls or indicators of fear. J Am Geriatr Soc. 1997;45:313–320. doi: 10.1111/j.1532-5415.1997.tb00946.x.
    1. Hausdorff JM, Rios DA, Edelberg HK. Gait variability and fall risk in community-living older adults: a 1-year prospective study. Arch Phys Med Rehabil. 2001;82:1050–1056. doi: 10.1053/apmr.2001.24893.
    1. Balasubramanian CK, Neptune RR, Kautz SA. Variability in spatiotemporal step characteristics and its relationship to walking performance post-stroke. Gait Posture. 2009;29:408–414. doi: 10.1016/j.gaitpost.2008.10.061.
    1. Hausdorff JM. Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos (Woodbury, N.Y.) 2009;19:026113. doi: 10.1063/1.3147408.
    1. Dubois B, Slachevsky A, Litvan I, Pillon B. The FAB: a Frontal Assessment Battery at bedside. Neurology. 2000;55:1621–1626. doi: 10.1212/WNL.55.11.1621.
    1. Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM. Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005;57(Suppl. 3):S4–16. doi: 10.1227/01.NEU.0000168185.29659.C5.
    1. Kang Y, Na DL, Hahn S. A validity study on the Korean Mini-Mental State Examination (K-MMSE) in dementia patients. J Korean Neurol Assoc. 1997;15:300–308.
    1. Choi SH, et al. Estimating the validity of the Korean version of expanded Clinical Dementia Rating (CDR) scale. J Korean Neurol Assoc. 2001;19:585–591.
    1. Kubo Y, et al. Validation of grading scale for evaluating symptoms of idiopathic normal-pressure hydrocephalus. Dement Geriatr Cogn Disord. 2008;25:37–45. doi: 10.1159/000111149.
    1. Rossier P, Wade DT. Validity and reliability comparison of 4 mobility measures in patients presenting with neurologic impairment. Arch Phys Med Rehabil. 2001;82:9–13. doi: 10.1053/apmr.2001.9396.
    1. Podsiadlo D, Richardson S. The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc. 1991;39:142–148. doi: 10.1111/j.1532-5415.1991.tb01616.x.
    1. Bohannon RW, Andrews AW, Thomas MW. Walking speed: reference values and correlates for older adults. J Orthop Sports Phys Ther. 1996;24:86–90. doi: 10.2519/jospt.1996.24.2.86.
    1. 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. Fluids Barriers CNS. 2012;9:1. doi: 10.1186/2045-8118-9-1.
    1. Hausdorff JM, Edelberg HK, Mitchell SL, Goldberger AL, Wei JY. Increased gait unsteadiness in community-dwelling elderly fallers. Arch Phys Med Rehabil. 1997;78:278–283. doi: 10.1016/s0003-9993(97)90034-4.
    1. Selge C, et al. Gait analysis in PSP and NPH: Dual-task conditions make the difference. Neurology. 2018;90:e1021–e1028. doi: 10.1212/WNL.0000000000005168.
    1. Nakamura T, et al. Postural and gait disturbance correlated with decreased frontal cerebral blood flow in Alzheimer disease. Alzheimer Dis Assoc Disord. 1997;11:132–139. doi: 10.1097/00002093-199709000-00005.
    1. Tian Q, et al. The brain map of gait variability in aging, cognitive impairment and dementia-A systematic review. Neuroscience and biobehavioral reviews. 2017;74:149–162. doi: 10.1016/j.neubiorev.2017.01.020.
    1. Denays R, Tondeur M, Noel P, Ham HR. Bilateral cerebral mediofrontal hypoactivity in Tc-99m HMPAO SPECT imaging. Clin Nucl Med. 1994;19:873–876. doi: 10.1097/00003072-199410000-00006.
    1. Kanno S, et al. White matter involvement in idiopathic normal pressure hydrocephalus: a voxel-based diffusion tensor imaging study. J Neurol. 2011;258:1949–1957. doi: 10.1007/s00415-011-6038-5.
    1. Guedj E, et al. Frontal Assessment Battery is a marker of dorsolateral and medial frontal functions: A SPECT study in frontotemporal dementia. J Neurol Sci. 2008;273:84–87. doi: 10.1016/j.jns.2008.06.035.
    1. Espay AJ, Narayan RK, Duker AP, Barrett ET, Jr., de Courten-Myers G. Lower-body parkinsonism: reconsidering the threshold for external lumbar drainage. Nat Clin Pract Neurol. 2008;4:50–55. doi: 10.1038/ncpneuro0688.
    1. Gallia GL, Rigamonti D, Williams MA. The diagnosis and treatment of idiopathic normal pressure hydrocephalus. Nat Clin Pract Neurol. 2006;2:375–381. doi: 10.1038/ncpneuro0237.
    1. Obeso JA, et al. The basal ganglia in Parkinson’s disease: current concepts and unexplained observations. Ann Neurol. 2008;64(Suppl 2):S30–46. doi: 10.1002/ana.21481.
    1. Wu T, et al. Basal ganglia circuits changes in Parkinson’s disease patients. Neurosci Lett. 2012;524:55–59. doi: 10.1016/j.neulet.2012.07.012.
    1. Lee PH, Yong SW, Ahn YH, Huh K. Correlation of midbrain diameter and gait disturbance in patients with idiopathic normal pressure hydrocephalus. J Neurol. 2005;252:958–963. doi: 10.1007/s00415-005-0791-2.
    1. Curran T, Lang AE. Parkinsonian syndromes associated with hydrocephalus: case reports, a review of the literature, and pathophysiological hypotheses. Mov Disord. 1994;9:508–520. doi: 10.1002/mds.870090503.
    1. Tohgi H, et al. Cerebral blood flow and oxygen metabolism in senile dementia of Alzheimer’s type and vascular dementia with deep white matter changes. Neuroradiology. 1998;40:131–137. doi: 10.1007/s002340050553.
    1. Mosconi MW, Wang Z, Schmitt LM, Tsai P, Sweeney JA. The role of cerebellar circuitry alterations in the pathophysiology of autism spectrum disorders. Front Neurosci. 2015;9:296. doi: 10.3389/fnins.2015.00296.
    1. Kwon MS, Kwon YR, Park YS, Kim JW. Comparison of gait patterns in elderly fallers and non-fallers. Technol Health Care. 2018;26:427–436. doi: 10.3233/THC-174736.
    1. Klarica M, Rados M, Oreskovic D. The Movement of Cerebrospinal Fluid and Its Relationship with Substances Behavior in Cerebrospinal and Interstitial Fluid. Neuroscience. 2019;414:28–48. doi: 10.1016/j.neuroscience.2019.06.032.
    1. Oreskovic D, Rados M, Klarica M. Role of choroid plexus in cerebrospinal fluid hydrodynamics. Neuroscience. 2017;354:69–87. doi: 10.1016/j.neuroscience.2017.04.025.
    1. Ziegelitz D, et al. Pre-and postoperative cerebral blood flow changes in patients with idiopathic normal pressure hydrocephalus measured by computed tomography (CT)-perfusion. J Cereb Blood Flow Metab. 2016;36:1755–1766. doi: 10.1177/0271678X15608521.
    1. Meyer JS, et al. Pathogenesis of normal-pressure hydrocephalus–preliminary observations. Surg Neurol. 1985;23:121–133. doi: 10.1016/0090-3019(85)90329-5.
    1. Lenfeldt N, et al. Idiopathic normal pressure hydrocephalus: increased supplementary motor activity accounts for improvement after CSF drainage. Brain. 2008;131:2904–2912. doi: 10.1093/brain/awn232.
    1. Kang K, Ko PW, Jin M, Suk K, Lee HW. Idiopathic normal-pressure hydrocephalus, cerebrospinal fluid biomarkers, and the cerebrospinal fluid tap test. J Clin Neurosci. 2014;21:1398–1403. doi: 10.1016/j.jocn.2013.11.039.

Source: PubMed

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구독하다