People with vestibular hypofunction (PwVH) often demonstrate abnormal gait and increased fall risk. An analysis of the strategies used for maintaining walking balance is lacking in PwVH.
Objective
The purpose of this study was to examine how PwVH use recovery strategies and maintain stability following perturbations.
Methods
PwVH and healthy controls were perturbed during walking with mediolateral ground shifts while kinematic responses were recorded.
Results
As a group, PwVH (n = 9, unilateral loss) responded similarly to healthy participants (n = 15) with changes in foot placement, ankle inversion, ankle push-off, and trunk sway. However, responses in PwVH depended on the vestibular lesion side and functional compensation as assessed by the Functional Gait Assessment (FGA). PwVH had larger changes in stability when perturbations caused body movement toward the side of the lesion and more effective trunk responses when perturbations caused body movement away from the lesion. Additionally, PwVH who performed poorly on the FGA showed worse stability and overactive ankle and trunk responses following medial perturbations.
Conclusions
These findings demonstrate kinematic differences in balance recovery in PwVH and suggest that PwVH are more susceptible to instability when falling toward the lesion.
BaubyCEKuoAD. Active control of lateral balance in human walking. J Biomech2000; 33: 1433–1440.
2.
KuoAD. Stabilization of lateral motion in passive dynamic walking. Int J Robot Res1999; 18: 917–930.
3.
ReimannHFettrowTGrenetD, et al.Phase-dependency of medial-lateral balance responses to sensory perturbations during walking. Front Sports Act Living2019; 1: 25.
4.
ReimannHFettrowTJekaJJ. Strategies for the control of balance during locomotion. Kinesiol Rev2018; 7: 18–25.
5.
ReimannHFettrowTThompsonED, et al.Neural control of balance during walking. Front Physiol2018; 9: 1271.
BestANWuAR. Upper body and ankle strategies compensate for reduced lateral stability at very slow walking speeds. Proc Biol Sci2020; 287: 20201685.
8.
BruijnSMVan DieënJH. Control of human gait stability through foot placement. J R Soc Interface2018; 15: 20170816.
9.
FettrowTDiBiancaSVanderlinde dos SantosF, et al.Flexible recruitment of balance mechanisms to environmental constraints during walking. Front virtual real2020; 1: 5.
10.
FettrowTReimannHGrenetD, et al.Walking cadence affects the recruitment of the medial-lateral balance mechanisms. Front Sports Act Living2019; 1: 40.
11.
KimMCollinsSH. Stabilization of a three-dimensional limit cycle walking model through step-to-step ankle control. In: 2013 IEEE 13th international conference on rehabilitation robotics (ICORR). IEEE, 2013, pp. 1–6.
12.
MahakiMBruijnSMvan DieënJH. The effect of external lateral stabilization on the use of foot placement to control mediolateral stability in walking and running. PeerJ2019; 7: e7939.
13.
ReimannHFettrowTDThompsonED, et al.Complementary mechanisms for upright balance during walking. PLoS One2017; 12: e0172215.
14.
ReimannHRamadanRFettrowT, et al.Interactions between different age-related factors affecting balance control in walking. Front Sports Act Living2020; 2: 94.
15.
AgrawalYMerfeldDMHorakFB, et al.Aging, vestibular function, and balance: proceedings of a National Institute on Aging/National Institute on Deafness and Other Communication Disorders workshop. J Gerontol A Biol Sci Med Sci2020; 75: 2471–2480.
16.
AgrawalYCareyJPDella SantinaCC, et al.Disorders of balance and vestibular function in US adults: data from the national health and nutrition examination survey, 2001–2004. Arch Intern Med2009; 169: 938–944.
17.
BentLRInglisJTMcFadyenBJ. When is vestibular information important during walking?J Neurophysiol2004; 92: 1269–1275.
18.
GrouvelGBoutablaACorreJ, et al.Full-body kinematics and head stabilisation strategies during walking in patients with chronic unilateral and bilateral vestibulopathy. Sci Rep2024; 14: 11757.
19.
GroveCRWhitneySLPyleGM, et al.Instrumented gait analysis to identify persistent deficits in gait stability in adults with chronic vestibular loss. JAMA Otolaryngol Head Neck Surg2021; 147: 729–738.
20.
LiuPHuangQOuY, et al.Characterizing patients with unilateral vestibular hypofunction using kinematic variability and local dynamic stability during treadmill walking. Behav Neurol2017; 2017: 4820428.
21.
LoydBJSaviers-SteigerJFangmanA, et al.Control of linear head and trunk acceleration during gait after unilateral vestibular deficits. Arch Phys Med Rehabil2021; 102: 456–462.
22.
MarchettiGFWhitneySLBlattPJ, et al.Temporal and spatial characteristics of gait during performance of the dynamic gait index in people with and people without balance or vestibular disorders. Phys Ther2008; 88: 640–651.
23.
GrouvelGBoutablaAArmandS, et al.Impaired spatiotemporal gait parameters in patients with unilateral and bilateral vestibular deficits. Gait Posture2023; 106: S70–S71.
24.
McCrumCEysel‐GosepathKEproG, et al.Deficient recovery response and adaptive feedback potential in dynamic gait stability in unilateral peripheral vestibular disorder patients. Physiological Reports2014; 2: e12222.
25.
WallCIIIOddssonLPatronikN, et al.Recovery trajectories of vestibulopathic subjects after perturbations during locomotion. J Vestib Res2002; 12: 239–253.
26.
HofADuysensJ. Responses of human ankle muscles to mediolateral balance perturbations during walking. Hum Mov Sci2018; 57: 69–82.
27.
HofAL. The equations of motion for a standing human reveal three mechanisms for balance. J Biomech2007; 40: 451–457.
28.
van LeeuwenAMvan DieënJHDaffertshoferA, et al.Ankle muscles drive mediolateral center of pressure control to ensure stable steady state gait. Sci Rep2021; 11: 21481.
29.
IshikawaKCaoZWWangY, et al.Dynamic locomotor function in normals and patients with vertigo. Acta Otolaryngol2001; 121: 241–244.
30.
HoogvlietPvan DuylWAde BakkerJV, et al.A model for the relation between the displacement of the ankle and the center of pressure in the frontal plane, during one-leg stance. Gait Posture1997; 6: 39–49.
31.
WhitneySLMarchettiGFPritcherM, et al.Gaze stabilization and gait performance in vestibular dysfunction. Gait Posture2009; 29: 194–198.
32.
Van LeeuwenMBruijnSVan DieënJ. Stabilization of gait, mechanisms, and opportunities for training. SportRxiv2022. https://doi.org/10.51224/SRXIV.216
33.
CerchiaiNNavariESellari-FranceschiniS, et al.Predicting the outcome after acute unilateral vestibulopathy: analysis of vestibulo-ocular reflex gain and catch-up saccades. Otolaryngol Head Neck Surg2018; 158: 527–533.
34.
LacourMHelmchenCVidalP-P. Vestibular compensation: the neuro-otologist’s best friend. J Neurol2016; 263: 54–64.
35.
VerbecqueEWuytsFLVanspauwenR, et al.The Antwerp Vestibular Compensation Index (AVeCI): an index for vestibular compensation estimation, based on functional balance performance. Eur Arch Otorhinolaryngol2021; 278: 1755–1763.
36.
BorelLHarlayFLopezC, et al.Walking performance of vestibular-defective patients before and after unilateral vestibular neurotomy. Behav Brain Res2004; 150: 191–200.
37.
BorelLHarlayFMagnanJ, et al.Deficits and recovery of head and trunk orientation and stabilization after unilateral vestibular loss. Brain2002; 125: 880–894.
38.
HalmagyiGWeberKCurthoysI. Vestibular function after acute vestibular neuritis. Restor Neurol Neurosci2010; 28: 37–46.
39.
KarabinMJSmithRWSpartoPJ, et al.Balance strategies for recovery from perturbed overground walking. J Biomech2024; 162: 111898.
WrisleyDMMarchettiGFKuharskyDK, et al.Reliability, internal consistency, and validity of data obtained with the functional gait assessment. Phys Ther2004; 84: 906–918.
42.
NilsagårdYKollénLAxelssonH, et al.Functional gait assessment: reliability and validity in people with peripheral vestibular disorders. Int J Ther Rehabil2014; 21: 367–373.
43.
JacobsonGPNewmanCW. The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Surg1990; 116: 424–427.
44.
HofAGazendamMSinkeW. The condition for dynamic stability. J Biomech2005; 38: 1–8.
45.
GehringDWisslerSLohrerH, et al.Expecting ankle tilts and wearing an ankle brace influence joint control in an imitated ankle sprain mechanism during walking. Gait Posture2014; 39: 894–898.
46.
WutzkeCJSawickiGSLewekMD. The influence of a unilateral fixed ankle on metabolic and mechanical demands during walking in unimpaired young adults. J Biomech2012; 45: 2405–2410.
47.
SartorCAlderinkGGreenwaldH, et al.Critical kinematic events occurring in the trunk during walking. Hum Mov Sci1999; 18: 669–679.
48.
HerdmanSJClendanielR. Vestibular rehabilitation. Philadelphia, PA: F. A. Davis, 2014.
49.
HorakFB. Postural compensation for vestibular loss. Ann N Y Acad Sci2009; 1164: 76–81.
50.
Alvarez-OteroRPerez-FernandezN. The limits of stability in patients with unilateral vestibulopathy. Acta Otolaryngol2017; 137: 1051–1056.
51.
HermanTGiladiNGurevichT, et al.Gait instability and fractal dynamics of older adults with a “cautious” gait: why do certain older adults walk fearfully?Gait Posture2005; 21: 178–185.
52.
MihailovicASwenorBKFriedmanDS, et al.Gait implications of visual field damage from glaucoma. Transl Vis Sci Technol2017; 6: 23.
53.
SchnieppRSchlickCSchenkelF, et al.Clinical and neurophysiological risk factors for falls in patients with bilateral vestibulopathy. J Neurol2017; 264: 277–283.
54.
BroughLGKluteGKNeptuneRR. Biomechanical response to mediolateral foot-placement perturbations during walking. J Biomech2021; 116: 110213.
55.
OddssonLIEWallCMcPartlandMD, et al.Recovery from perturbations during paced walking. Gait Posture2004; 19: 24–34.
56.
NashnerLMBlackFOWallC. Adaptation to altered support and visual conditions during stance: patients with vestibular deficits. J Neurosci1982; 2: 536–544.
57.
LacourMBernard-DemanzeL. Interaction between vestibular compensation mechanisms and vestibular rehabilitation therapy: 10 recommendations for optimal functional recovery. Front Neurol2015; 5: 285.
58.
BruijnSMvan DieënJHMeijerOG, et al.Is slow walking more stable?J Biomech2009; 42: 1506–1512.
59.
DingwellJBMarinLC. Kinematic variability and local dynamic stability of upper body motions when walking at different speeds. J Biomech2006; 39: 444–452.
60.
DonkerSFBeekPJ. Interlimb coordination in prosthetic walking: effects of asymmetry and walking velocity. Acta Psychol2002; 110: 265–288.
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