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Assisted technology in Parkinson's disease gait: what's up?

Tecnologia assistida na marcha da doença de Parkinson: o que há de novo?

Abstract

Background

Gait disturbances are prevalent and debilitating symptoms, diminishing mobility and quality of life for Parkinson's disease (PD) individuals. While traditional treatments offer partial relief, there is a growing interest in alternative interventions to address this challenge. Recently, a remarkable surge in assisted technology (AT) development was witnessed to aid individuals with PD.

Objective

To explore the burgeoning landscape of AT interventions tailored to alleviate PD-related gait impairments and describe current research related to such aim.

Methods

In this review, we searched on PubMed for papers published in English (2018-2023). Additionally, the abstract of each study was read to ensure inclusion. Four researchers searched independently, including studies according to our inclusion and exclusion criteria.

Results

We included studies that met all inclusion criteria. We identified key trends in assistive technology of gait parameters analysis in PD. These encompass wearable sensors, gait analysis, real-time feedback and cueing techniques, virtual reality, and robotics.

Conclusion

This review provides a resource for guiding future research, informing clinical decisions, and fostering collaboration among researchers, clinicians, and policymakers. By delineating this rapidly evolving field's contours, it aims to inspire further innovation, ultimately improving the lives of PD patients through more effective and personalized interventions.

Keywords
Parkinson Disease; Gait Disorders; Neurologic; Neurological Rehabilitation; Self-Help Devices; Virtual Reality; Exoskeleton Device; Physical Therapy Modalities

Resumo

Antecedentes

Os distúrbios da marcha são sintomas prevalentes e debilitantes, diminuindo muito a mobilidade e a qualidade de vida dos indivíduos com doença de Parkinson (DP). Embora os tratamentos tradicionais ofereçam alívio parcial, há um interesse crescente em intervenções alternativas para enfrentar esse desafio. Recentemente, um aumento notável no desenvolvimento de tecnologia assistida (TA) foi testemunhado para ajudar indivíduos com DP.

Objetivo

Explorar o cenário crescente de intervenções de TA adaptadas para aliviar deficiências de marcha relacionadas à DP e descrever as pesquisas atuais para esse fim.

Métodos

Nessa revisão, pesquisamos artigos em inglês publicados no PubMed de 2018 a 2023. Além disso, os resumos de cada trabalho foram lidos para assegurar a sua inclusão. Quatro pesquisadores buscaram independentemente os artigos de acordo com os critérios de inclusão e exclusão.

Resultados

Incluímos trabalhos que preencheram os critérios de inclusão. Identificamos as tendências em tecnologia assistiva na análise dos parâmetros da marcha em DP. Esses compreendem os sensores portáteis, análise da marcha, retroalimentação em tempo real e técnicas de pista, realidade virtual e robótica.

Conclusão

Essa revisão é um recurso para orientar pesquisas futuras, informar decisões clínicas e promover a colaboração entre pesquisadores, médicos e formuladores de políticas. Ao delinear os contornos deste campo em rápida evolução, pretende inspirar mais inovação, melhorando em última análise a vida dos pacientes com DP através de intervenções mais eficazes e personalizadas.

Palavras-chave
Doença de Parkinson; Transtornos Neurológicos da Marcha; Reabilitação Neurológica; Tecnologia Assistiva; Realidade Virtual; Dispositivo Robótico; Exoesqueleto; Fisioterapia

INTRODUCTION

Parkinson's disease (PD) is a progressive neurodegenerative disorder affecting millions of individuals worldwide, significantly burdening patients and their caregivers.11 Bloem BR, Okun MS, Klein C. Parkinson’s disease. Lancet 2021;397 (10291):2284–2303 Among the myriad of symptoms associated with PD, gait disturbances are one of the most prevalent and debilitating, contributing to a substantial decline in the quality of life (QoL).22 Capato TTC. Clinical Assessment and Management of Balance Impairments in Parkinson's disease, in Donders Institute. 2022Radboud University Nijmegen, the Netherlands. p. 168. ISBN: 978–94–6423–873–0 Although many resources are available for the management of PD motor symptoms, gait impairment only partially benefits from antiparkinsonian drug treatment and surgical intervention.11 Bloem BR, Okun MS, Klein C. Parkinson’s disease. Lancet 2021;397 (10291):2284–2303,33 Saba RA, Maia DP, Cardoso FEC, et al. Guidelines for Parkinson’s disease treatment: consensus from the Movement Disorders Scientific Department of the Brazilian Academy of Neurologymotor symptoms. Arq Neuropsiquiatr 2022;80(03):316–329. Doi: 10.1590/0004-282X-ANP-2021-0219
https://doi.org/10.1590/0004-282X-ANP-20...

Assistive Technology (AT) is an umbrella term covering the systems and services related to the delivery of assistive products (AP) and services, enabling, and promoting the inclusion and participation of persons with disability, aging populations, and people with non-communicable diseases. Therefore, the use of AP may maintain or improve PD patients' functioning and independence, thereby promoting their well-being (WHO assistive - https://www.who.int/health-topics/assistive-technology#tab=tab_1). AT may be an asset in the rehabilitation program44 García-López H, Obrero-Gaitán E, Castro-Sánchez AM, Lara-Palomo IC, Nieto-Escamez FA, Cortés-Pérez I. Non-Immersive Virtual Reality to Improve Balance and Reduce Risk of Falls in People Diagnosed with Parkinson’s Disease: A Systematic Review. Brain Sci 2021;11(11):1435. Doi: 10.3390/brainsci11111435
https://doi.org/10.3390/brainsci11111435...
and development of devices enabling objective, accurate, and better gait assessment and monitoring is crucial for people with PD.55 García-Bustillo Á, Valiñas-Sieiro F, Allende-Río M, González-Santos J, Cubo Eand the Multidisciplinary Telemedicine Group. Assistive Devices for Personal Mobility in Parkinson’s Disease: A Systematic Review of the Literature. Mov Disord Clin Pract (Hoboken) 2022;9(08):1040–1046

In response to this pressing need, novel rehabilitation interventions and technology have emerged, offering new avenues for assisting individuals with PD in managing their gait difficulties.66 Osborne JA, Botkin R, Colon-Semenza C, et al. Physical Therapist Management of Parkinson Disease: A Clinical Practice Guideline From the American Physical Therapy Association. Phys Ther 2022; 102(04):pzab302. Doi: 10.1093/ptj/pzab302 Erratum in: Phys Ther. 2022 Aug 1;102(8): PMID: 34963139; PMCID: PMC9046970
https://doi.org/10.1093/ptj/pzab302...
,77 Espay AJ, Hausdorff JM, Sánchez-Ferro Á, et al; Movement Disorder Society Task Force on Technology. A roadmap for implementation of patient-centered digital outcome measures in Parkinson’s disease obtained using mobile health technologies. Mov Disord 2019;34(05):657–663. Doi: 10.1002/mds.27671
https://doi.org/10.1002/mds.27671...
The search for innovative interventions has led to the surge of numerous gait AP such as wearable devices,88 Silva de Lima AL, Hahn T, Evers LJW, et al. Feasibility of large-scale deployment of multiple wearable sensors in Parkinson’s disease. PLoS One 2017;12(12):e0189161. Doi: 10.1371/journal. pone.0189161
https://doi.org/10.1371/journal.pone.018...
robotic exoskeletons,99 Xue X, Yang X, Deng Z. Efficacy of rehabilitation robot-assisted gait training on lower extremity dyskinesia in patients with Parkinson’s disease: A systematic review and meta-analysis. Ageing Res Rev 2023;85:101837,1010 Alwardat M, Etoom M, Al Dajah S, et al. Effectiveness of robot-assisted gait training on motor impairments in people with Parkinson’s disease: a systematic review and meta-analysis. Int J Rehabil Res 2018;41(04):287–296. Doi: 10.1097/MRR.00 00000000000312
https://doi.org/10.1097/MRR.000000000000...
Robot-assisted and treadmill,1111 Picelli A, Melotti C, Origano F, Neri R, Waldner A, Smania N. Robot- assisted gait training versus equal intensity treadmill training in patients with mild to moderate Parkinson’s disease: a randomized controlled trial. Parkinsonism Relat Disord 2013;19(06): 605–610. Doi: 10.1016/j.parkreldis.2013.02.010
https://doi.org/10.1016/j.parkreldis.201...
virtual reality (VR),1212 Mirelman A, Rochester L, Maidan I, et al. Addition of a nonimmersive virtual reality component to treadmill training to reduce fall risk in older adults (V-TIME): a randomised controlled trial. Lancet 2016;388(10050):1170–1182. Doi: 10.1016/S01406736(16)31325-3
https://doi.org/10.1016/S0140-6736(16)31...
,1313 Janssen S, Bolte B, Nonnekes J, et al. Usability of Three-dimensional Augmented Visual Cues Delivered by Smart Glasses on (Freezing of) Gait in Parkinson’s Disease. Front Neurol 2017; 8:279. Doi: 10.3389/fneur.2017.00279
https://doi.org/10.3389/fneur.2017.00279...
exergames-based interventions,1414 Pompeu JE, Mendes FA, Silva KG, et al. Effect of Nintendo Wii™-based motor and cognitive training on activities of daily living in patients with Parkinson’s disease: a randomised clinical trial. Physiotherapy 2012;98(03):196–204. Doi: 10.1016/j.physio.2012.06.004
https://doi.org/10.1016/j.physio.2012.06...
smartphone or mobile health applications,1515 Ellis TD, Earhart GM. Digital Therapeutics in Parkinson’s Disease: Practical Applications and Future Potential. J Parkinsons Dis 2021; 11(s1):S95–S101. Doi: 10.3233/JPD-202407
https://doi.org/10.3233/JPD-202407...
and sensor-based systems1616 Silva de Lima AL, Smits T, Darweesh SKL, et al. Home-based monitoring of falls using wearable sensors in Parkinson’s disease. Mov Disord 2020;35(01):109–115. Doi: 10.1002/mds.27830
https://doi.org/10.1002/mds.27830...
among others. These AP, with diverse mechanisms of action, provide real-time feedback on gait parameters, promote targeted rehabilitative exercises, and may enhance overall gait performance.55 García-Bustillo Á, Valiñas-Sieiro F, Allende-Río M, González-Santos J, Cubo Eand the Multidisciplinary Telemedicine Group. Assistive Devices for Personal Mobility in Parkinson’s Disease: A Systematic Review of the Literature. Mov Disord Clin Pract (Hoboken) 2022;9(08):1040–1046,1515 Ellis TD, Earhart GM. Digital Therapeutics in Parkinson’s Disease: Practical Applications and Future Potential. J Parkinsons Dis 2021; 11(s1):S95–S101. Doi: 10.3233/JPD-202407
https://doi.org/10.3233/JPD-202407...

A better understanding of emerging AT to assess gait in PD is important since it continues to advance and become more available. However, keeping pace with rapidly evolving technologies is challenging. Recognizing the potential and utility of these AP for assessing or improving mobility will help consumers and researchers to better manage and broaden their applicability in rehabilitation or clinical practice.

Herein, this review aims to provide an overview of current AT interventions for PD gait rehabilitation. We hope to enable healthcare professionals to understand the available technologies and their clinical and rehabilitation applications. For this purpose, we compiled and synthesized the existing body of literature and selected studies that assessed the efficacy, usability, and acceptability of current technological interventions. We also explored the outcomes of recently published studies, including improvements in gait speed, balance, stride length, and fall risk of PD patients.

METHODS

Given the limited scientific evidence and the heterogeneity of the available studies in this field, we opted for a review to give an overview of the emerging body of literature on assistive devices to improve gait in PD.

Identification of studies, selection, and eligibility

This review was written according to the recommendations of Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR).1717 Tricco AC, Lillie E, Zarin W, et al. PRISMA Extension for Scoping Reviews (PRISMA-ScR): Checklist and Explanation. Ann Intern Med 2018;169(07):467–473

We searched on PubMed studies characterized as clinical trials (randomized and non-randomized), meta-analyses, systematic reviews, literature reviews, cross-sectional studies, cohort studies, and pilot studies. We looked for the following descriptors: assistive technology, assistive device, Parkinson's disease, gait disorders, gait analysis, wearable sensors, wearable devices, cueing, virtual reality, exergames, robotic-assisted gait.

We included only studies published in English and human subjects between October/2018 and October/2023. Additionally, the abstract of each study was read to ensure inclusion. All studies that did not mention Parkinson's disease or present technologies to assess or treat PD in the methodology were excluded (Figure 1).

Figure 1
Flow diagram of literature search strategy.

Four reviewers (T.C., J.C., J.A., H.C.) screened titles and abstracts by inclusion and exclusion criteria. The authors worked in pairs and solved disagreements (if there were any) before the study inclusion.

RESULTS

We only included studies that met all inclusion criteria after analyzing their respective titles, abstracts, and texts. In total, we selected 412 studies. We included 72 studies that met all inclusion criteria. Several types of technological devices used to evaluate and treat gait in Parkinson's disease were identified.

We found several assistive technology devices for gait analysis, and they are used to identify and diagnose gait and other motor symptoms (EEG, EMG, Azure Kinect, HTC VIVE VR; GAITRite Portable Walkway System),1818 Spanakis M, Xylouri I, Patelarou E, Patelarou A. A Literature Review of High-Tech Physiotherapy Interventions in the Elderly with Neurological Disorders. Int J Environ Res Public Health 2022; 19(15):9233. Doi: 10.3390/ijerph19159233
https://doi.org/10.3390/ijerph19159233...

19 Peng K, Xie L, Hong R, et al. Early-onset and late-onset Parkinson’s disease exhibit a different profile of gait and posture features based on the Kinect. Neurol Sci 2023;•••: Epub ahead of print. Doi: 10.1007/s10072-023-07009-y
https://doi.org/10.1007/s10072-023-07009...

20 Bansal SK, Basumatary B, Bansal R, Sahani AK. Techniques for the detection and management of freezing of gait in Parkinson’s disease - A systematic review and future perspectives. MethodsX 2023;10:102106. Doi: 10.1016/j.mex.2023.102106
https://doi.org/10.1016/j.mex.2023.10210...
-2121 Yamagami M, Imsdahl S, Lindgren K, et al. Effects of virtual reality environments on overground walking in people with Parkinson disease and freezing of gait. Disabil Rehabil Assist Technol 2023; 18(03):266–273. Doi: 10.1080/17483107.2020.1842920
https://doi.org/10.1080/17483107.2020.18...
to track gait and motor symptoms (VIBE),2222 Lu M, Zhao Q, Poston KL, et al. Quantifying Parkinson’s disease motor severity under uncertainty using MDS-UPDRS videos. Med Image Anal 2021;73:102179. Doi: 10.1016/j.media.2021.102179
https://doi.org/10.1016/j.media.2021.102...
,2323 Lu M, Poston K, Pfefferbaum A, et al. Vision-based Estimation of MDS-UPDRS Gait Scores for Assessing Parkinson’s Disease Motor Severity. Med Image Comput Comput Assist Interv 2020; 12263:637–647. Doi: 10.1007/978-3-030-59716-0_61
https://doi.org/10.1007/978-3-030-59716-...
and to treat gait (Keeogo Reha exoskeleton, Tymo system; Treadmills, Gait Trainer GT1, Lokomat, Cycle Ergometers, Walkbot-S, Non-motorized treadmill, G-EO system, SMART Lounge vibroacoustic system, Smart shoes, XaviX system, App "PatientConcept").1818 Spanakis M, Xylouri I, Patelarou E, Patelarou A. A Literature Review of High-Tech Physiotherapy Interventions in the Elderly with Neurological Disorders. Int J Environ Res Public Health 2022; 19(15):9233. Doi: 10.3390/ijerph19159233
https://doi.org/10.3390/ijerph19159233...
,2424 Gryfe P, Sexton A, McGibbon CA. Using gait robotics to improve symptoms of Parkinson’s disease: an open-label, pilot randomized controlled trial. Eur J Phys Rehabil Med 2022;58(05): 723–737. Doi: 10.23736/S1973-9087.22.07549-9
https://doi.org/10.23736/S1973-9087.22.0...

25 Maranesi E, Casoni E, Baldoni R, et al. The Effect of Non-Immersive Virtual Reality Exergames versus Traditional Physiotherapy in Parkinson’s Disease Older Patients: Preliminary Results from a Randomized-Controlled Trial. Int J Environ Res Public Health 2022;19(22):14818. Doi: 10.3390/ijerph192214818
https://doi.org/10.3390/ijerph192214818...

26 Yun SJ, Lee HH, Lee WH, Lee SH, Oh BM, Seo HG. Effect of robot-assisted gait training on gait automaticity in Parkinson disease: A prospective, open-label, single-arm, pilot study. Medicine (Baltimore) 2021;100(05):e24348. Doi: 10.1097/ MD.0000000000024348
https://doi.org/10.1097/MD.0000000000024...

27 Fundarò C, Maestri R, Ferriero G, Chimento P, Taveggia G, Casale R. Self-selected speed gait training in Parkinson’s disease: robot- assisted gait training with virtual reality versus gait training on the ground. Eur J Phys Rehabil Med 2019;55(04):456–462. Doi: 10.23736/S1973-9087.18.05368-6
https://doi.org/10.23736/S1973-9087.18.0...

28 Penn IW, Sung WH, Lin PH, et al. Speed and temporal adaptations during nonmotorized treadmill walking in Parkinson disease and nondisabled individuals. Int J Rehabil Res 2019;42(02):126–132. Doi: 10.1097/MRR.0000000000000334
https://doi.org/10.1097/MRR.000000000000...
-2929 Capecci M, Pournajaf S, Galafate D, et al. Clinical effects of robot- assisted gait training and treadmill training for Parkinson’s disease. A randomized controlled trial. Ann Phys Rehabil Med 2019;62(05):303–312. Doi: 10.1016/j.rehab.2019.06.016
https://doi.org/10.1016/j.rehab.2019.06....

The most frequently used systems in gait analysis are motion capture systems (3D systems, multi-sensors combined or optoelectronic systems, 3D systems, multi-sensors combined or optoelectronic systems),2020 Bansal SK, Basumatary B, Bansal R, Sahani AK. Techniques for the detection and management of freezing of gait in Parkinson’s disease - A systematic review and future perspectives. MethodsX 2023;10:102106. Doi: 10.1016/j.mex.2023.102106
https://doi.org/10.1016/j.mex.2023.10210...
,2121 Yamagami M, Imsdahl S, Lindgren K, et al. Effects of virtual reality environments on overground walking in people with Parkinson disease and freezing of gait. Disabil Rehabil Assist Technol 2023; 18(03):266–273. Doi: 10.1080/17483107.2020.1842920
https://doi.org/10.1080/17483107.2020.18...
inertial Measurement Unit (IMU)2020 Bansal SK, Basumatary B, Bansal R, Sahani AK. Techniques for the detection and management of freezing of gait in Parkinson’s disease - A systematic review and future perspectives. MethodsX 2023;10:102106. Doi: 10.1016/j.mex.2023.102106
https://doi.org/10.1016/j.mex.2023.10210...
,3030 Han Y, Liu X, Zhang N, et al. Automatic Assessments of Parkinsonian Gait with Wearable Sensors for Human Assistive Systems. Sensors (Basel) 2023;23(04):2104. Doi: 10.3390/s23042104
https://doi.org/10.3390/s23042104...
; and force plates.2020 Bansal SK, Basumatary B, Bansal R, Sahani AK. Techniques for the detection and management of freezing of gait in Parkinson’s disease - A systematic review and future perspectives. MethodsX 2023;10:102106. Doi: 10.1016/j.mex.2023.102106
https://doi.org/10.1016/j.mex.2023.10210...
Other studies monitoring gait parameters in PD used wearable sensors or wearable devices based on different types of sensors.3131 Laar A, Silva de Lima AL, Maas BR, Bloem BR, de Vries NM. Successful implementation of technology in the management of Parkinson’s disease: Barriers and facilitators. Clin Park Relat Disord 2023;8:100188. Doi: 10.1016/j.prdoa.2023.100188
https://doi.org/10.1016/j.prdoa.2023.100...

32 Brognara L, Palumbo P, Grimm B, Palmerini L. Assessing Gait in Parkinson’s Disease Using Wearable Motion Sensors: A Systematic Review. Diseases 2019;7(01):18. Doi: 10.3390/diseases7010018
https://doi.org/10.3390/diseases7010018...

33 Guo Y, Yang J, Liu Y, Chen X, Yang GZ. Detection and assessment of Parkinson’s disease based on gait analysis: A survey. Front Aging Neurosci 2022;14:916971. Doi: 10.3389/fnagi.2022.916971
https://doi.org/10.3389/fnagi.2022.91697...

34 Mate KKV, Abou-Sharkh A, Mansoubi M, et al. Evidence for the Efficacy of Commercially Available Wearable Biofeedback Gait Devices: Consumer-Centered Review. JMIR Rehabil Assist Technol 2023;10:e40680. Doi: 10.2196/40680
https://doi.org/10.2196/40680...

35 Tsakanikas V, Ntanis A, Rigas G, et al. Evaluating Gait Impairment in Parkinson’s Disease from Instrumented Insole and IMU Sensor Data. Sensors (Basel) 2023;23(08):3902. Doi: 10.3390/s23083902
https://doi.org/10.3390/s23083902...

36 Zhu S, Wu Z, Wang Y, et al. Gait Analysis with Wearables Is a Potential Progression Marker in Parkinson’s Disease. Brain Sci 2022;12(09):1213. Doi: 10.3390/brainsci12091213
https://doi.org/10.3390/brainsci12091213...

37 Nóbrega LR, Rocon E, Pereira AA, Andrade AO. A Novel Physical Mobility Task to Assess Freezers in Parkinson’s Disease. Healthcare (Basel) 2023;11(03):409. Doi: 10.3390/healthcare11030409
https://doi.org/10.3390/healthcare110304...

38 Marcante A, Di Marco R, Gentile G, et al. Foot Pressure Wearable Sensors for Freezing of Gait Detection in Parkinson’s Disease. Sensors (Basel) 2020;21(01):128. Doi: 10.3390/s21010128
https://doi.org/10.3390/s21010128...
-3939 di Biase L, Raiano L, Caminiti ML, Pecoraro PM, Di Lazzaro V. Parkinson’s Disease Wearable Gait Analysis: Kinematic and Dynamic Markers for Diagnosis. Sensors (Basel) 2022;22(22):8773. Doi: 10.3390/s22228773
https://doi.org/10.3390/s22228773...

Two guideline reviews emphasized the high level of evidence of cueing techniques using real feedback to improve gait performance.33 Saba RA, Maia DP, Cardoso FEC, et al. Guidelines for Parkinson’s disease treatment: consensus from the Movement Disorders Scientific Department of the Brazilian Academy of Neurologymotor symptoms. Arq Neuropsiquiatr 2022;80(03):316–329. Doi: 10.1590/0004-282X-ANP-2021-0219
https://doi.org/10.1590/0004-282X-ANP-20...
,66 Osborne JA, Botkin R, Colon-Semenza C, et al. Physical Therapist Management of Parkinson Disease: A Clinical Practice Guideline From the American Physical Therapy Association. Phys Ther 2022; 102(04):pzab302. Doi: 10.1093/ptj/pzab302 Erratum in: Phys Ther. 2022 Aug 1;102(8): PMID: 34963139; PMCID: PMC9046970
https://doi.org/10.1093/ptj/pzab302...
We also found some studies using devices as compensation strategies to improve gait in PD such as visual laser cues,4040 Barthel C, Nonnekes J, van Helvert M, et al. The laser shoes: A new ambulatory device to alleviate freezing of gait in Parkinson disease. Neurology 2018;90(02):e164–e171. Doi: 10.1212/ WNL.0000000000004795
https://doi.org/10.1212/WNL.000000000000...
rhythmical auditory cues provided by a metronome,4141 Capato TTC, de Vries NM, IntHout J, Barbosa ER, Nonnekes J, Bloem BR. Multimodal Balance Training Supported by Rhythmical Auditory Stimuli in Parkinson’s Disease: A Randomized Clinical Trial. J Parkinsons Dis 2020;10(01):333–346. Doi: 10.3233/JPD-191752
https://doi.org/10.3233/JPD-191752...
and tactile cues.4242 Klaver EC, van Vugt JPP, Bloem BR, van Wezel RJA, Nonnekes J, Tjepkema-Cloostermans MC. Good vibrations: tactile cueing for freezing of gait in Parkinson’s disease. J Neurol 2023;270(07): 3424–3432. Doi: 10.1007/s00415-023-11663-9
https://doi.org/10.1007/s00415-023-11663...

Some studies used VR to interact three-dimensional virtual environment.44 García-López H, Obrero-Gaitán E, Castro-Sánchez AM, Lara-Palomo IC, Nieto-Escamez FA, Cortés-Pérez I. Non-Immersive Virtual Reality to Improve Balance and Reduce Risk of Falls in People Diagnosed with Parkinson’s Disease: A Systematic Review. Brain Sci 2021;11(11):1435. Doi: 10.3390/brainsci11111435
https://doi.org/10.3390/brainsci11111435...
,2525 Maranesi E, Casoni E, Baldoni R, et al. The Effect of Non-Immersive Virtual Reality Exergames versus Traditional Physiotherapy in Parkinson’s Disease Older Patients: Preliminary Results from a Randomized-Controlled Trial. Int J Environ Res Public Health 2022;19(22):14818. Doi: 10.3390/ijerph192214818
https://doi.org/10.3390/ijerph192214818...
,4343 Santos P, Machado T, Santos L, Ribeiro N, Melo A. Efficacy of the Nintendo Wii combination with Conventional Exercises in the rehabilitation of individuals with Parkinson’s disease: A randomized clinical trial. NeuroRehabilitation 2019;45(02):255–263

44 Pazzaglia C, Imbimbo I, Tranchita E, et al. Comparison of virtual reality rehabilitation and conventional rehabilitation in Parkinson’s disease: a randomised controlled trial. Physiotherapy 2020; 106:36–42. Doi: 10.1016/j.physio.2019.12.007
https://doi.org/10.1016/j.physio.2019.12...

45 Bekkers EMJ, Mirelman A, Alcock L, et al. Do Patients With Parkinson’s Disease With Freezing of Gait Respond Differently Than Those Without to Treadmill Training Augmented by Virtual Reality? Neurorehabil Neural Repair 2020;34(05):440–449. Doi: 10.1177/1545968320912756
https://doi.org/10.1177/1545968320912756...

46 Pelosin E, Ponte C, Putzolu M, et al. Motor-Cognitive Treadmill Training With Virtual Reality in Parkinson’s Disease: The Effect of Training Duration. Front Aging Neurosci 2022;13:753381. Doi: 10.3389/fnagi.2021.753381
https://doi.org/10.3389/fnagi.2021.75338...

47 Hajebrahimi F, Velioglu HA, Bayraktaroglu Z, Helvaci Yilmaz N, Hanoglu L. Clinical evaluation and resting state fMRI analysis of virtual reality based training in Parkinson’s disease through a randomized controlled trial. Sci Rep 2022;12(01):8024. Doi: 10.1038/s41598-022-12061-3
https://doi.org/10.1038/s41598-022-12061...

48 Feitosa JA, Fernandes CA, Casseb RF, Castellano G. Effects of virtual reality-based motor rehabilitation: a systematic review of fMRI studies. J Neural Eng 2022;19(01):. Doi: 10.1088/1741-2552/ac456e
https://doi.org/10.1088/1741-2552/ac456e...

49 Freitag F, Brucki SMD, Barbosa AF, et al. Is virtual reality beneficial for dual-task gait training in patients with Parkinson’s disease? A systematic review. Dement Neuropsychol 2019;13(03):259–267. Doi: 10.1590/1980-57642018dn13-030002
https://doi.org/10.1590/1980-57642018dn1...

50 Lei C, Sunzi K, Dai F, et al. Effects of virtual reality rehabilitation training on gait and balance in patients with Parkinson’s disease: A systematic review. PLoS One 2019;14(11):e0224819. Doi: 10.1371/journal.pone.0224819
https://doi.org/10.1371/journal.pone.022...

51 Kashif M, Ahmad A, Bandpei MAM, Farooq M, Iram H, E Fatima R. Systematic review of the application of virtual reality to improve balance, gait and motor function in patients with Parkinson’s disease. Medicine (Baltimore) 2022;101(31):e29212. Doi: 10.1097/MD.0000000000029212
https://doi.org/10.1097/MD.0000000000029...

52 Kwon SH, Park JK, Koh YH. A systematic review and meta-analysis on the effect of virtual reality-based rehabilitation for people with Parkinson’s disease. J Neuroeng Rehabil 2023;20(01):94. Doi: 10.1186/s12984-023-01219-3
https://doi.org/10.1186/s12984-023-01219...

53 Abd-Alrazaq A, Alhuwail D, Al-Jafar E, et al. The Effectiveness of Serious Games in Improving Memory Among Older Adults With Cognitive Impairment: Systematic Review and Meta-analysis. JMIR Serious Games 2022;10(03):e35202

54 Wu J, Zhang H, Chen Z, et al. Benefits of Virtual Reality Balance Training for Patients With Parkinson Disease: Systematic Review, Meta-analysis, and Meta-Regression of a Randomized Controlled Trial. JMIR Serious Games 2022;10(01):e30882. Doi: 10.2196/30882
https://doi.org/10.2196/30882...

55 Li R, Zhang Y, Jiang Y, Wang M, Ang WHD, Lau Y. Rehabilitation training based on virtual reality for patients with Parkinson’s disease in improving balance, quality of life, activities of daily living, and depressive symptoms: A systematic review and metaregression analysis. Clin Rehabil 2021;35(08):1089–1102. Doi: 10.1177/0269215521995179
https://doi.org/10.1177/0269215521995179...

56 Sarasso E, Gardoni A, Tettamanti A, Agosta F, Filippi M, Corbetta D. Virtual reality balance training to improve balance and mobility in Parkinson’s disease: a systematic review and meta-analysis. J Neurol 2022;269(04):1873–1888. Doi: 10.1007/s00415-02110857-3
https://doi.org/10.1007/s00415-021-10857...

57 Navarro-Lozano F, Kiper P, Carmona-Pérez C, Rutkowski S, Pinero- Pinto E, Luque-Moreno C. Effects of Non-Immersive Virtual Reality and Video Games on Walking Speed in Parkinson Disease: A Systematic Review and Meta-Analysis. J Clin Med 2022;11(22): 6610. Doi: 10.3390/jcm11226610
https://doi.org/10.3390/jcm11226610...
-5858 Brandín-De la Cruz N, Secorro N, Calvo S, Benyoucef Y, Herrero P, Bellosta-López P. Immersive virtual reality and antigravity treadmill training for gait rehabilitation in Parkinson’s disease: a pilot and feasibility study. Rev Neurol 2020;71(12):447–454. Doi: 10.33588/rn.7112.2020352
https://doi.org/10.33588/rn.7112.2020352...

We also found studies using Robotic-assisted gait training for PD.2424 Gryfe P, Sexton A, McGibbon CA. Using gait robotics to improve symptoms of Parkinson’s disease: an open-label, pilot randomized controlled trial. Eur J Phys Rehabil Med 2022;58(05): 723–737. Doi: 10.23736/S1973-9087.22.07549-9
https://doi.org/10.23736/S1973-9087.22.0...
,2929 Capecci M, Pournajaf S, Galafate D, et al. Clinical effects of robot- assisted gait training and treadmill training for Parkinson’s disease. A randomized controlled trial. Ann Phys Rehabil Med 2019;62(05):303–312. Doi: 10.1016/j.rehab.2019.06.016
https://doi.org/10.1016/j.rehab.2019.06....
,5959 Kim H, Kim E, Yun SJ, et al. Robot-assisted gait training with auditory and visual cues in Parkinson’s disease: A randomized controlled trial. Ann Phys Rehabil Med 2022;65(03):101620. Doi: 10.1016/j.rehab.2021.101620
https://doi.org/10.1016/j.rehab.2021.101...

60 Kawashima N, Hasegawa K, Iijima M, et al. Efficacy of Wearable Device Gait Training on Parkinson’s Disease: A Randomized Controlled Open-label Pilot Study. Intern Med 2022;61(17): 2573–2580. Doi: 10.2169/internalmedicine.8949-21
https://doi.org/10.2169/internalmedicine...

61 Alwardat M, Etoom M. Effectiveness of robot-assisted gait training on freezing of gait in people with Parkinson disease: evidence from a literature review. J Exerc Rehabil 2019;15(02):187–192. Doi: 10.12965/jer.1836618.309
https://doi.org/10.12965/jer.1836618.309...
-6262 Fujii C, Wakizaka N, Araki Y, Tashiro K, Endou M. Video analysis ofsafety and reproducibility issues with the timed up-and-go test applied to patients with Parkinson’s disease. Disabil Rehabil Assist Technol 2022; 17(07):801–806. Doi: 10.1080/17483107.2020.1817990
https://doi.org/10.1080/17483107.2020.18...

We analyzed several types of AP and categorized them into commercial and non-commercial devices available for research, rehabilitation, or home-based care. The majority of them are available on the market and depicted in Table 1. To make for easy reading, and based on the interventions that were described, we subdivided our findings into the following subtopics: wearable sensors, gait analysis, real-time feedback and cueing techniques, VR, and robotics.

Table 1
Overview of tradeable and non-tradeable devices

DISCUSSION

Wearable sensors

The advancement of sensor technology, motion capture systems, and force platforms have been employed as more objective and precise methods for evaluating PD patient's gait.3333 Guo Y, Yang J, Liu Y, Chen X, Yang GZ. Detection and assessment of Parkinson’s disease based on gait analysis: A survey. Front Aging Neurosci 2022;14:916971. Doi: 10.3389/fnagi.2022.916971
https://doi.org/10.3389/fnagi.2022.91697...
Sensor and Wearable devices (SWD) facilitate and monitor an individual's activity. They are an important asset for intervention and monitoring and are easy to integrate into the patients' daily routines.3131 Laar A, Silva de Lima AL, Maas BR, Bloem BR, de Vries NM. Successful implementation of technology in the management of Parkinson’s disease: Barriers and facilitators. Clin Park Relat Disord 2023;8:100188. Doi: 10.1016/j.prdoa.2023.100188
https://doi.org/10.1016/j.prdoa.2023.100...
SWD enables the remote assessment of patients' conditions in their natural environment, promoting a more comprehensive clinical evaluation and empowering patients to monitor their gait.

Most of the SWD sensors to analyze spatio-temporal parameters of gait in patients with PD were placed on both ankles and tibias, feet, chest, and lower back. For gait parameters, speed was the most common feature evaluated, followed by cadence, stride length, and stride time. For step characteristics, step time, step length, and right-left asymmetry were mostly assessed.3232 Brognara L, Palumbo P, Grimm B, Palmerini L. Assessing Gait in Parkinson’s Disease Using Wearable Motion Sensors: A Systematic Review. Diseases 2019;7(01):18. Doi: 10.3390/diseases7010018
https://doi.org/10.3390/diseases7010018...

Many low-cost devices have been employed to collect real-time spatiotemporal, kinematic, and kinetic gait features in PD patients. Costly force platforms used to measure ground reaction force during gait may be replaced by pressure insole. These insoles are composed of an accelerometer, gyroscope, and sometimes a magnetometer attached to the patient and can measure the linear and angular velocity, acceleration, and other gait parameters.3535 Tsakanikas V, Ntanis A, Rigas G, et al. Evaluating Gait Impairment in Parkinson’s Disease from Instrumented Insole and IMU Sensor Data. Sensors (Basel) 2023;23(08):3902. Doi: 10.3390/s23083902
https://doi.org/10.3390/s23083902...
Sensors may also be placed under smart shoes and inertial microelectromechanical system sensors attached to the patients to measure stride length, gait velocity, range of motion of the ankle, knee, and hip joints of individuals with PD.3636 Zhu S, Wu Z, Wang Y, et al. Gait Analysis with Wearables Is a Potential Progression Marker in Parkinson’s Disease. Brain Sci 2022;12(09):1213. Doi: 10.3390/brainsci12091213
https://doi.org/10.3390/brainsci12091213...
Other studies are focusing on developing new SWD to detect the occurrence of freezing of gait (FOG) and its discrimination in PD (freezing, shuffling, and trembling),3737 Nóbrega LR, Rocon E, Pereira AA, Andrade AO. A Novel Physical Mobility Task to Assess Freezers in Parkinson’s Disease. Healthcare (Basel) 2023;11(03):409. Doi: 10.3390/healthcare11030409
https://doi.org/10.3390/healthcare110304...
and promising resources may be launched in the near future.3838 Marcante A, Di Marco R, Gentile G, et al. Foot Pressure Wearable Sensors for Freezing of Gait Detection in Parkinson’s Disease. Sensors (Basel) 2020;21(01):128. Doi: 10.3390/s21010128
https://doi.org/10.3390/s21010128...

These AP have also been tested to discriminate PD individuals from healthy controls. A recent study explored which parameter could discriminate PD from controls, and they observed that kinematic features were more informative than kinetic analysis.3939 di Biase L, Raiano L, Caminiti ML, Pecoraro PM, Di Lazzaro V. Parkinson’s Disease Wearable Gait Analysis: Kinematic and Dynamic Markers for Diagnosis. Sensors (Basel) 2022;22(22):8773. Doi: 10.3390/s22228773
https://doi.org/10.3390/s22228773...
Smartphones are a promising tool to discriminate gait and postural instability between healthy controls and individuals with PD.6363 Abou L, Peters J, Wong E, et al. Gait and Balance Assessments using Smartphone Applications in Parkinson’s Disease: A Systematic Review. J Med Syst 2021;45(09):87. Doi: 10.1007/s10916-02101760-5
https://doi.org/10.1007/s10916-021-01760...
However, it has also been used to promote home-based gait training, so future research should investigate the role of smartphones as an AP for home-based rehabilitation support.

Moving arms in a rhythmic and symmetrical contributes to postural stability and walking efficiency. SWD may also be placed on the upper limb and are useful to measure the arms arm swing during walking. One trial used a motion-capture system computer with speech models and advanced artificial intelligence sensors for orientation and spatial tracking to collect 3-dimension joint trajectories and body segments during walking. The authors could quantify arm swing features as well as lower gait velocity of PD patients compared to healthy controls, thus offering a simple tool to provide a more comprehensive gait assessment.6464 Ferraris C, Amprimo G, Masi G, et al. Evaluation of Arm Swing Features and Asymmetry during Gait in Parkinson’s Disease Using the Azure Kinect Sensor. Sensors (Basel) 2022;22(16):6282. Doi: 10.3390/s22166282
https://doi.org/10.3390/s22166282...
,6565 Brand YE, Schwartz D, Gazit E, Buchman AS, Gilad-Bachrach R, Hausdorff JM. Gait Detection from a Wrist-Worn Sensor Using Machine Learning Methods: A Daily Living Study in Older Adults and People with Parkinson’s Disease. Sensors (Basel) 2022;22 (18):7094. Doi: 10.3390/s22187094
https://doi.org/10.3390/s22187094...

A recent consumer-centered review described the available commercial SWD targeting improvement in gait patterns and walking behavior. Of the 11 commercially available devices, only 4 (36%) had findable evidence for efficacy potential supporting the claims.3434 Mate KKV, Abou-Sharkh A, Mansoubi M, et al. Evidence for the Efficacy of Commercially Available Wearable Biofeedback Gait Devices: Consumer-Centered Review. JMIR Rehabil Assist Technol 2023;10:e40680. Doi: 10.2196/40680
https://doi.org/10.2196/40680...
Although there are promising results with SWD for gait assessment, many challenges need to be overcome. To cite some, gait requires complex algorithms for its analysis, and most of the available portable devices do not avoid noise contamination or provide precise data synchronization and collection of real-time spatiotemporal, kinematic, and kinetic parameters. Available SWD capture short walking bouts and good gait quality measures cannot rely on short interval data. Moreover, gait assessment obtained from laboratory machine learning methods does not necessarily reflect gait features in patients' daily living. New algorithms and sensor detectors resolution improvements are needed to accurately extract facets of gait quality and function.6464 Ferraris C, Amprimo G, Masi G, et al. Evaluation of Arm Swing Features and Asymmetry during Gait in Parkinson’s Disease Using the Azure Kinect Sensor. Sensors (Basel) 2022;22(16):6282. Doi: 10.3390/s22166282
https://doi.org/10.3390/s22166282...
Future devices should be sensitive to precisely distinguish between healthy controls and early or mild symptomatic PD patients and also provide accurate gait parameters enabling early intervention of patients with a higher risk for falling or FOG.

Gait analysis

Emerging technology for gait analysis aims to identify and diagnose abnormal gait parameters in PD, but it may also be used to monitor and improve gait, balance, and mobility.77 Espay AJ, Hausdorff JM, Sánchez-Ferro Á, et al; Movement Disorder Society Task Force on Technology. A roadmap for implementation of patient-centered digital outcome measures in Parkinson’s disease obtained using mobile health technologies. Mov Disord 2019;34(05):657–663. Doi: 10.1002/mds.27671
https://doi.org/10.1002/mds.27671...
Currently, most of the devices used for gait analysis can be categorized into a) motion capture systems (3D systems, multi-sensors combined or optoelectronic systems); b) inertial measurement unit; and c) force plates.2020 Bansal SK, Basumatary B, Bansal R, Sahani AK. Techniques for the detection and management of freezing of gait in Parkinson’s disease - A systematic review and future perspectives. MethodsX 2023;10:102106. Doi: 10.1016/j.mex.2023.102106
https://doi.org/10.1016/j.mex.2023.10210...
,2222 Lu M, Zhao Q, Poston KL, et al. Quantifying Parkinson’s disease motor severity under uncertainty using MDS-UPDRS videos. Med Image Anal 2021;73:102179. Doi: 10.1016/j.media.2021.102179
https://doi.org/10.1016/j.media.2021.102...
,3030 Han Y, Liu X, Zhang N, et al. Automatic Assessments of Parkinsonian Gait with Wearable Sensors for Human Assistive Systems. Sensors (Basel) 2023;23(04):2104. Doi: 10.3390/s23042104
https://doi.org/10.3390/s23042104...
,6666 Zhang M, Artan NS, Gu H, et al. Gait Study of Parkinson’s Disease Subjects Using Haptic Cues with A Motorized Walker. Sensors (Basel) 2018;18(10):3549. Doi: 10.3390/s18103549
https://doi.org/10.3390/s18103549...

Most of the trials for gait analysis evaluated its speed with good reliability. The Berg Balance Scale and UPDRS part III were often used for outcome ratings. Overall, the AP were well accepted by the patients.1010 Alwardat M, Etoom M, Al Dajah S, et al. Effectiveness of robot-assisted gait training on motor impairments in people with Parkinson’s disease: a systematic review and meta-analysis. Int J Rehabil Res 2018;41(04):287–296. Doi: 10.1097/MRR.00 00000000000312
https://doi.org/10.1097/MRR.000000000000...
,1818 Spanakis M, Xylouri I, Patelarou E, Patelarou A. A Literature Review of High-Tech Physiotherapy Interventions in the Elderly with Neurological Disorders. Int J Environ Res Public Health 2022; 19(15):9233. Doi: 10.3390/ijerph19159233
https://doi.org/10.3390/ijerph19159233...
,2222 Lu M, Zhao Q, Poston KL, et al. Quantifying Parkinson’s disease motor severity under uncertainty using MDS-UPDRS videos. Med Image Anal 2021;73:102179. Doi: 10.1016/j.media.2021.102179
https://doi.org/10.1016/j.media.2021.102...

23 Lu M, Poston K, Pfefferbaum A, et al. Vision-based Estimation of MDS-UPDRS Gait Scores for Assessing Parkinson’s Disease Motor Severity. Med Image Comput Comput Assist Interv 2020; 12263:637–647. Doi: 10.1007/978-3-030-59716-0_61
https://doi.org/10.1007/978-3-030-59716-...

24 Gryfe P, Sexton A, McGibbon CA. Using gait robotics to improve symptoms of Parkinson’s disease: an open-label, pilot randomized controlled trial. Eur J Phys Rehabil Med 2022;58(05): 723–737. Doi: 10.23736/S1973-9087.22.07549-9
https://doi.org/10.23736/S1973-9087.22.0...

25 Maranesi E, Casoni E, Baldoni R, et al. The Effect of Non-Immersive Virtual Reality Exergames versus Traditional Physiotherapy in Parkinson’s Disease Older Patients: Preliminary Results from a Randomized-Controlled Trial. Int J Environ Res Public Health 2022;19(22):14818. Doi: 10.3390/ijerph192214818
https://doi.org/10.3390/ijerph192214818...

26 Yun SJ, Lee HH, Lee WH, Lee SH, Oh BM, Seo HG. Effect of robot-assisted gait training on gait automaticity in Parkinson disease: A prospective, open-label, single-arm, pilot study. Medicine (Baltimore) 2021;100(05):e24348. Doi: 10.1097/ MD.0000000000024348
https://doi.org/10.1097/MD.0000000000024...
-2727 Fundarò C, Maestri R, Ferriero G, Chimento P, Taveggia G, Casale R. Self-selected speed gait training in Parkinson’s disease: robot- assisted gait training with virtual reality versus gait training on the ground. Eur J Phys Rehabil Med 2019;55(04):456–462. Doi: 10.23736/S1973-9087.18.05368-6
https://doi.org/10.23736/S1973-9087.18.0...
Other parameters frequently assessed in the studies besides gait speed were: step length, step symmetry, falls and freezing of gait.2828 Penn IW, Sung WH, Lin PH, et al. Speed and temporal adaptations during nonmotorized treadmill walking in Parkinson disease and nondisabled individuals. Int J Rehabil Res 2019;42(02):126–132. Doi: 10.1097/MRR.0000000000000334
https://doi.org/10.1097/MRR.000000000000...

29 Capecci M, Pournajaf S, Galafate D, et al. Clinical effects of robot- assisted gait training and treadmill training for Parkinson’s disease. A randomized controlled trial. Ann Phys Rehabil Med 2019;62(05):303–312. Doi: 10.1016/j.rehab.2019.06.016
https://doi.org/10.1016/j.rehab.2019.06....
-3030 Han Y, Liu X, Zhang N, et al. Automatic Assessments of Parkinsonian Gait with Wearable Sensors for Human Assistive Systems. Sensors (Basel) 2023;23(04):2104. Doi: 10.3390/s23042104
https://doi.org/10.3390/s23042104...
,6666 Zhang M, Artan NS, Gu H, et al. Gait Study of Parkinson’s Disease Subjects Using Haptic Cues with A Motorized Walker. Sensors (Basel) 2018;18(10):3549. Doi: 10.3390/s18103549
https://doi.org/10.3390/s18103549...
Assistive devices obtained significant correlations on PD gait analysis in at least one of the above-mentioned parameters. However, the effectiveness of these AP and the outcomes are variables since they cannot yet overcome laboratory gait conventional monitoring or replace validated PD gait assessment tests or scales. Still, some commercial devices have been efficacious for the analysis and treatment of gait and balance in PD.1010 Alwardat M, Etoom M, Al Dajah S, et al. Effectiveness of robot-assisted gait training on motor impairments in people with Parkinson’s disease: a systematic review and meta-analysis. Int J Rehabil Res 2018;41(04):287–296. Doi: 10.1097/MRR.00 00000000000312
https://doi.org/10.1097/MRR.000000000000...
,1818 Spanakis M, Xylouri I, Patelarou E, Patelarou A. A Literature Review of High-Tech Physiotherapy Interventions in the Elderly with Neurological Disorders. Int J Environ Res Public Health 2022; 19(15):9233. Doi: 10.3390/ijerph19159233
https://doi.org/10.3390/ijerph19159233...
,2020 Bansal SK, Basumatary B, Bansal R, Sahani AK. Techniques for the detection and management of freezing of gait in Parkinson’s disease - A systematic review and future perspectives. MethodsX 2023;10:102106. Doi: 10.1016/j.mex.2023.102106
https://doi.org/10.1016/j.mex.2023.10210...
,2727 Fundarò C, Maestri R, Ferriero G, Chimento P, Taveggia G, Casale R. Self-selected speed gait training in Parkinson’s disease: robot- assisted gait training with virtual reality versus gait training on the ground. Eur J Phys Rehabil Med 2019;55(04):456–462. Doi: 10.23736/S1973-9087.18.05368-6
https://doi.org/10.23736/S1973-9087.18.0...

Many AP devices not only assess but are also ancillary for gait and balance rehabilitation treatment. In this aspect, gait assistance robots (GAR), such as the G-EO system, Gait Trainer GT1, Lokomat, and GAITRite are the preferred equipment for this purpose.1010 Alwardat M, Etoom M, Al Dajah S, et al. Effectiveness of robot-assisted gait training on motor impairments in people with Parkinson’s disease: a systematic review and meta-analysis. Int J Rehabil Res 2018;41(04):287–296. Doi: 10.1097/MRR.00 00000000000312
https://doi.org/10.1097/MRR.000000000000...
,1818 Spanakis M, Xylouri I, Patelarou E, Patelarou A. A Literature Review of High-Tech Physiotherapy Interventions in the Elderly with Neurological Disorders. Int J Environ Res Public Health 2022; 19(15):9233. Doi: 10.3390/ijerph19159233
https://doi.org/10.3390/ijerph19159233...
,2727 Fundarò C, Maestri R, Ferriero G, Chimento P, Taveggia G, Casale R. Self-selected speed gait training in Parkinson’s disease: robot- assisted gait training with virtual reality versus gait training on the ground. Eur J Phys Rehabil Med 2019;55(04):456–462. Doi: 10.23736/S1973-9087.18.05368-6
https://doi.org/10.23736/S1973-9087.18.0...
,2929 Capecci M, Pournajaf S, Galafate D, et al. Clinical effects of robot- assisted gait training and treadmill training for Parkinson’s disease. A randomized controlled trial. Ann Phys Rehabil Med 2019;62(05):303–312. Doi: 10.1016/j.rehab.2019.06.016
https://doi.org/10.1016/j.rehab.2019.06....
Another gait treatment strategy is to combine traditional treadmill training with assessment assistive devices.1818 Spanakis M, Xylouri I, Patelarou E, Patelarou A. A Literature Review of High-Tech Physiotherapy Interventions in the Elderly with Neurological Disorders. Int J Environ Res Public Health 2022; 19(15):9233. Doi: 10.3390/ijerph19159233
https://doi.org/10.3390/ijerph19159233...
Before long, more walking aid gadgets and innovative AP will be launched on the market combining both evaluation and treatment strategies2828 Penn IW, Sung WH, Lin PH, et al. Speed and temporal adaptations during nonmotorized treadmill walking in Parkinson disease and nondisabled individuals. Int J Rehabil Res 2019;42(02):126–132. Doi: 10.1097/MRR.0000000000000334
https://doi.org/10.1097/MRR.000000000000...
and more trials will be necessary to explore their plausibility and effectiveness in clinical practice.

Despite the promising potential of assisted technology for gait analysis, several challenges and questions remain unaddressed.6767 Evers LJW, Peeters JM, Bloem BR, Meinders MJ. Need for personalized monitoring of Parkinson’s disease: the perspectives of patients and specialized healthcare providers. Front Neurol 2023;14:1150634. Doi: 10.3389/fneur.2023.1150634
https://doi.org/10.3389/fneur.2023.11506...
Several barriers may be listed for its limited utilization as a gait rehabilitation tool such as high cost, unfamiliarity with technology, technical issues, low usability, and so on. Being so, strategies to increase awareness and make this resource generally available are welcome and may help to broaden assistive devices accessibility for research, clinical, and consumers use. As an example, in the last years, there has been an increasing process for portability and miniaturization of mobile health technologies.77 Espay AJ, Hausdorff JM, Sánchez-Ferro Á, et al; Movement Disorder Society Task Force on Technology. A roadmap for implementation of patient-centered digital outcome measures in Parkinson’s disease obtained using mobile health technologies. Mov Disord 2019;34(05):657–663. Doi: 10.1002/mds.27671
https://doi.org/10.1002/mds.27671...

Furthermore, ethical concerns regarding data privacy, patient autonomy, and equitable access to technology must be examined in-depth. Additionally, the use of these devices and outcomes on the role of telehealth and remote monitoring in delivering personalized gait analysis programs requires further exploration, especially in the context of evolving healthcare practices and digital health solutions. So, due to the complexity of PD gait management, perhaps advances in artificial intelligence may, in near future, promote, refine analyses, and support treatment strategies in PD gait rehabilitation.

Real-time feedback and cueing techniques (auditory, visual, and proprioceptive)

The positive effects of the cues on gait performance (speed, cadence, step length, and stride) are well recognized and supported by a robust level of evidence.33 Saba RA, Maia DP, Cardoso FEC, et al. Guidelines for Parkinson’s disease treatment: consensus from the Movement Disorders Scientific Department of the Brazilian Academy of Neurologymotor symptoms. Arq Neuropsiquiatr 2022;80(03):316–329. Doi: 10.1590/0004-282X-ANP-2021-0219
https://doi.org/10.1590/0004-282X-ANP-20...
,66 Osborne JA, Botkin R, Colon-Semenza C, et al. Physical Therapist Management of Parkinson Disease: A Clinical Practice Guideline From the American Physical Therapy Association. Phys Ther 2022; 102(04):pzab302. Doi: 10.1093/ptj/pzab302 Erratum in: Phys Ther. 2022 Aug 1;102(8): PMID: 34963139; PMCID: PMC9046970
https://doi.org/10.1093/ptj/pzab302...
External cues, such as auditory and visual ones, are used to bypass and compensate for the brain's abnormal internal cueing mechanisms that cause deficiencies in movement planning and execution in PD.22 Capato TTC. Clinical Assessment and Management of Balance Impairments in Parkinson's disease, in Donders Institute. 2022Radboud University Nijmegen, the Netherlands. p. 168. ISBN: 978–94–6423–873–0

These compensation strategies (or cueing techniques) delivered by physiotherapists, such as multimodal training, may provide feedback, repetition, and high challenges and can be used to correct temporal aspects of gait, improve balance and walking speed and prevent freezing episodes.4141 Capato TTC, de Vries NM, IntHout J, Barbosa ER, Nonnekes J, Bloem BR. Multimodal Balance Training Supported by Rhythmical Auditory Stimuli in Parkinson’s Disease: A Randomized Clinical Trial. J Parkinsons Dis 2020;10(01):333–346. Doi: 10.3233/JPD-191752
https://doi.org/10.3233/JPD-191752...
It has been demonstrated that people with PD training with audio cues, such as a digital metronome improve balance and gait performance.4141 Capato TTC, de Vries NM, IntHout J, Barbosa ER, Nonnekes J, Bloem BR. Multimodal Balance Training Supported by Rhythmical Auditory Stimuli in Parkinson’s Disease: A Randomized Clinical Trial. J Parkinsons Dis 2020;10(01):333–346. Doi: 10.3233/JPD-191752
https://doi.org/10.3233/JPD-191752...
Besides, cueing training may overcome or ameliorate FOG episodes in the short and long term.6868 Capato TTC, de Vries NM, IntHout J, et al. Multimodal Balance Training Supported by Rhythmic Auditory Stimuli in Parkinson Disease: Effects in Freezers and Nonfreezers. Phys Ther 2020;100 (11):2023–2034. Doi: 10.1093/ptj/pzaa146
https://doi.org/10.1093/ptj/pzaa146...
Moreover, cueing may be applied to different mobile health applications,1515 Ellis TD, Earhart GM. Digital Therapeutics in Parkinson’s Disease: Practical Applications and Future Potential. J Parkinsons Dis 2021; 11(s1):S95–S101. Doi: 10.3233/JPD-202407
https://doi.org/10.3233/JPD-202407...
and digital devices such as robot-assisted rhythmic cues5959 Kim H, Kim E, Yun SJ, et al. Robot-assisted gait training with auditory and visual cues in Parkinson’s disease: A randomized controlled trial. Ann Phys Rehabil Med 2022;65(03):101620. Doi: 10.1016/j.rehab.2021.101620
https://doi.org/10.1016/j.rehab.2021.101...
or laser attached to patient's shoes (the laser shoes).4040 Barthel C, Nonnekes J, van Helvert M, et al. The laser shoes: A new ambulatory device to alleviate freezing of gait in Parkinson disease. Neurology 2018;90(02):e164–e171. Doi: 10.1212/ WNL.0000000000004795
https://doi.org/10.1212/WNL.000000000000...

Additionally, proprioceptive devices, such as tactile cues or vibratory ones, are being explored to provide external support during walking.4242 Klaver EC, van Vugt JPP, Bloem BR, van Wezel RJA, Nonnekes J, Tjepkema-Cloostermans MC. Good vibrations: tactile cueing for freezing of gait in Parkinson’s disease. J Neurol 2023;270(07): 3424–3432. Doi: 10.1007/s00415-023-11663-9
https://doi.org/10.1007/s00415-023-11663...
Finally, visual, and auditory cues can be combined with treadmill training, and it has shown to be better than standard treadmill training alone.4646 Pelosin E, Ponte C, Putzolu M, et al. Motor-Cognitive Treadmill Training With Virtual Reality in Parkinson’s Disease: The Effect of Training Duration. Front Aging Neurosci 2022;13:753381. Doi: 10.3389/fnagi.2021.753381
https://doi.org/10.3389/fnagi.2021.75338...
This association may focus on gait and cognitive deficits to optimally address several critical aspects of fall risk and improve mobility, physical activity, cognitive function, and FOG in PD.

Virtual reality

VR is a computer technology that enables users to interact in a three-dimensional (3D) virtual environment and experience similar situations in the real world. This technology facilitates the perception of physical movements and visual, auditory, and tactile input. VR can be categorized into three types according to the degree of immersion: non-immersive,44 García-López H, Obrero-Gaitán E, Castro-Sánchez AM, Lara-Palomo IC, Nieto-Escamez FA, Cortés-Pérez I. Non-Immersive Virtual Reality to Improve Balance and Reduce Risk of Falls in People Diagnosed with Parkinson’s Disease: A Systematic Review. Brain Sci 2021;11(11):1435. Doi: 10.3390/brainsci11111435
https://doi.org/10.3390/brainsci11111435...
semi-immersive,5252 Kwon SH, Park JK, Koh YH. A systematic review and meta-analysis on the effect of virtual reality-based rehabilitation for people with Parkinson’s disease. J Neuroeng Rehabil 2023;20(01):94. Doi: 10.1186/s12984-023-01219-3
https://doi.org/10.1186/s12984-023-01219...
and full-immersive.6363 Abou L, Peters J, Wong E, et al. Gait and Balance Assessments using Smartphone Applications in Parkinson’s Disease: A Systematic Review. J Med Syst 2021;45(09):87. Doi: 10.1007/s10916-02101760-5
https://doi.org/10.1007/s10916-021-01760...
In a non-immersive system, the patient can interact with the virtual environment using a computer screen and game console.44 García-López H, Obrero-Gaitán E, Castro-Sánchez AM, Lara-Palomo IC, Nieto-Escamez FA, Cortés-Pérez I. Non-Immersive Virtual Reality to Improve Balance and Reduce Risk of Falls in People Diagnosed with Parkinson’s Disease: A Systematic Review. Brain Sci 2021;11(11):1435. Doi: 10.3390/brainsci11111435
https://doi.org/10.3390/brainsci11111435...
A semi-immersive VR system consists of large screens or projections to enable a visual-virtual 3D-space experience and uses interactive devices such as a motion tracker, haptic gloves, and balance platform.5252 Kwon SH, Park JK, Koh YH. A systematic review and meta-analysis on the effect of virtual reality-based rehabilitation for people with Parkinson’s disease. J Neuroeng Rehabil 2023;20(01):94. Doi: 10.1186/s12984-023-01219-3
https://doi.org/10.1186/s12984-023-01219...
Fully immersive VR incorporates the combination of more sophisticated graphic systems to create a virtual world and advanced wearable devices. It allows users to safely and effectively experience motor challenging situations at their own pace and difficulty level and can observe their performance in real-time, receiving immediate feedback regarding movement and balance control.6969 Yun SJ, Hyun SE, Oh BM, Seo HG. Fully immersive virtual reality exergames with dual-task components for patients with Parkinson’s disease: a feasibility study. J Neuroeng Rehabil 2023;20(01): 92. Doi: 10.1186/s12984-023-01215-7
https://doi.org/10.1186/s12984-023-01215...

Exergame is the gamification of rehabilitation using electronic games that capture and simulate real movements. It requires the participants to be physically active or exercise and apply full body motion to play the games.7070 Chuang CS, Chen YW, Zeng BY, et al. Effects of modern technology (exergame and virtual reality) assisted rehabilitation vs conventional rehabilitation in patients with Parkinson’s disease: a network meta-analysis of randomised controlled trials. Physiotherapy 2022; 117:35–42. Doi: 10.1016/j.physio.2022.07.001
https://doi.org/10.1016/j.physio.2022.07...
It is a low-cost and accessible approach for healthcare professionals to incorporate this training in rehabilitation programs. Examples of exergames resources are Nintendo Wii, Kinect, and games designed for computers or sensors like Leap Motion.7070 Chuang CS, Chen YW, Zeng BY, et al. Effects of modern technology (exergame and virtual reality) assisted rehabilitation vs conventional rehabilitation in patients with Parkinson’s disease: a network meta-analysis of randomised controlled trials. Physiotherapy 2022; 117:35–42. Doi: 10.1016/j.physio.2022.07.001
https://doi.org/10.1016/j.physio.2022.07...
Therapy based on commercial video games increases patients' motivation, provides direct feedback, and allows dual-task training.4949 Freitag F, Brucki SMD, Barbosa AF, et al. Is virtual reality beneficial for dual-task gait training in patients with Parkinson’s disease? A systematic review. Dement Neuropsychol 2019;13(03):259–267. Doi: 10.1590/1980-57642018dn13-030002
https://doi.org/10.1590/1980-57642018dn1...
This exercise modality appears to benefit functional circuitry in PD and facilitates learning through reinforcement feedback.6969 Yun SJ, Hyun SE, Oh BM, Seo HG. Fully immersive virtual reality exergames with dual-task components for patients with Parkinson’s disease: a feasibility study. J Neuroeng Rehabil 2023;20(01): 92. Doi: 10.1186/s12984-023-01215-7
https://doi.org/10.1186/s12984-023-01215...
The training approach promotes sensory input, central integration, coordination, weight transfer, and balance, with subsequent improvements in muscle control and coordination, and might improve motor function in neurological disorders.5353 Abd-Alrazaq A, Alhuwail D, Al-Jafar E, et al. The Effectiveness of Serious Games in Improving Memory Among Older Adults With Cognitive Impairment: Systematic Review and Meta-analysis. JMIR Serious Games 2022;10(03):e35202

Studies have shown that short-term exergame associated or not with conventional training may improve QoL,4343 Santos P, Machado T, Santos L, Ribeiro N, Melo A. Efficacy of the Nintendo Wii combination with Conventional Exercises in the rehabilitation of individuals with Parkinson’s disease: A randomized clinical trial. NeuroRehabilitation 2019;45(02):255–263 postural instability, balance,4444 Pazzaglia C, Imbimbo I, Tranchita E, et al. Comparison of virtual reality rehabilitation and conventional rehabilitation in Parkinson’s disease: a randomised controlled trial. Physiotherapy 2020; 106:36–42. Doi: 10.1016/j.physio.2019.12.007
https://doi.org/10.1016/j.physio.2019.12...
,5454 Wu J, Zhang H, Chen Z, et al. Benefits of Virtual Reality Balance Training for Patients With Parkinson Disease: Systematic Review, Meta-analysis, and Meta-Regression of a Randomized Controlled Trial. JMIR Serious Games 2022;10(01):e30882. Doi: 10.2196/30882
https://doi.org/10.2196/30882...
mobility, gait parameters, and reduced risk of falls in PD.2525 Maranesi E, Casoni E, Baldoni R, et al. The Effect of Non-Immersive Virtual Reality Exergames versus Traditional Physiotherapy in Parkinson’s Disease Older Patients: Preliminary Results from a Randomized-Controlled Trial. Int J Environ Res Public Health 2022;19(22):14818. Doi: 10.3390/ijerph192214818
https://doi.org/10.3390/ijerph192214818...
These findings were endorsed by a systematic review in which exergame training reduced the number of falls and improved static and dynamic balance in patients with PD.44 García-López H, Obrero-Gaitán E, Castro-Sánchez AM, Lara-Palomo IC, Nieto-Escamez FA, Cortés-Pérez I. Non-Immersive Virtual Reality to Improve Balance and Reduce Risk of Falls in People Diagnosed with Parkinson’s Disease: A Systematic Review. Brain Sci 2021;11(11):1435. Doi: 10.3390/brainsci11111435
https://doi.org/10.3390/brainsci11111435...
It is worth highlighting that in order to improve balance, a supervised VR program might require at least 20 minutes, 4 to 6 times a week of training5454 Wu J, Zhang H, Chen Z, et al. Benefits of Virtual Reality Balance Training for Patients With Parkinson Disease: Systematic Review, Meta-analysis, and Meta-Regression of a Randomized Controlled Trial. JMIR Serious Games 2022;10(01):e30882. Doi: 10.2196/30882
https://doi.org/10.2196/30882...
and that younger patients have better outcomes than older ones.5555 Li R, Zhang Y, Jiang Y, Wang M, Ang WHD, Lau Y. Rehabilitation training based on virtual reality for patients with Parkinson’s disease in improving balance, quality of life, activities of daily living, and depressive symptoms: A systematic review and metaregression analysis. Clin Rehabil 2021;35(08):1089–1102. Doi: 10.1177/0269215521995179
https://doi.org/10.1177/0269215521995179...
The longer-term efficacy of VR and exergames interventions is still unclear, therefore, more trials are needed to address these questions.

Immersive VR with body weight supported treadmill warrants PD patients to exercise in a safer condition. It provides repetitive, task-oriented, and higher-intensity training. The association of both apparatuses with a 20% body weight support improves gait and balance assessment.5858 Brandín-De la Cruz N, Secorro N, Calvo S, Benyoucef Y, Herrero P, Bellosta-López P. Immersive virtual reality and antigravity treadmill training for gait rehabilitation in Parkinson’s disease: a pilot and feasibility study. Rev Neurol 2020;71(12):447–454. Doi: 10.33588/rn.7112.2020352
https://doi.org/10.33588/rn.7112.2020352...
Moreover, those who trained with the treadmill and VR had fewer falls than those with the treadmill only, but no changes were found for FOG.4545 Bekkers EMJ, Mirelman A, Alcock L, et al. Do Patients With Parkinson’s Disease With Freezing of Gait Respond Differently Than Those Without to Treadmill Training Augmented by Virtual Reality? Neurorehabil Neural Repair 2020;34(05):440–449. Doi: 10.1177/1545968320912756
https://doi.org/10.1177/1545968320912756...
The benefit may vary according to training duration, PD patients who underwent a 12-week exercise program had better gait speed, stride length under dual-task conditions, and falls reduction compared to a 6-week VR training.4646 Pelosin E, Ponte C, Putzolu M, et al. Motor-Cognitive Treadmill Training With Virtual Reality in Parkinson’s Disease: The Effect of Training Duration. Front Aging Neurosci 2022;13:753381. Doi: 10.3389/fnagi.2021.753381
https://doi.org/10.3389/fnagi.2021.75338...

So far, most of the studies evidenced that VR rehabilitation may have beneficial effects on balance. In relation to gait, improvements in speed, step length, and cadence in both kinematics and clinical scale tests were observed,4949 Freitag F, Brucki SMD, Barbosa AF, et al. Is virtual reality beneficial for dual-task gait training in patients with Parkinson’s disease? A systematic review. Dement Neuropsychol 2019;13(03):259–267. Doi: 10.1590/1980-57642018dn13-030002
https://doi.org/10.1590/1980-57642018dn1...
but no significant differences were seen in walking speed in PD.5656 Sarasso E, Gardoni A, Tettamanti A, Agosta F, Filippi M, Corbetta D. Virtual reality balance training to improve balance and mobility in Parkinson’s disease: a systematic review and meta-analysis. J Neurol 2022;269(04):1873–1888. Doi: 10.1007/s00415-02110857-3
https://doi.org/10.1007/s00415-021-10857...
On the other hand, a meta-analysis showed no statistically significant differences in gait ability, activity of daily living, motor function, and QoL in PD after VR training.5757 Navarro-Lozano F, Kiper P, Carmona-Pérez C, Rutkowski S, Pinero- Pinto E, Luque-Moreno C. Effects of Non-Immersive Virtual Reality and Video Games on Walking Speed in Parkinson Disease: A Systematic Review and Meta-Analysis. J Clin Med 2022;11(22): 6610. Doi: 10.3390/jcm11226610
https://doi.org/10.3390/jcm11226610...
It is noteworthy that a meta-regression analysis utilizing publication year as the predictor variable showed a greater improvement in balance function in recent studies compared with older ones. This could be attributed to the technological advancement. VR has become cheaper and more accessible, enabling more patient enrollment in trials and resulting in greater data accessibility.

Studies observed that VR rehabilitation may improve neuroplasticity and change brain neural patterns by activation and reorganization mainly of the primary motor cortex, sensorimotor cortex, and supplementary motor area.4848 Feitosa JA, Fernandes CA, Casseb RF, Castellano G. Effects of virtual reality-based motor rehabilitation: a systematic review of fMRI studies. J Neural Eng 2022;19(01):. Doi: 10.1088/1741-2552/ac456e
https://doi.org/10.1088/1741-2552/ac456e...
In addition, functional magnetic resonance imaging showed that PD patients who underwent VR training increased activity in the precuneus region, which is linked to visuospatial integration, memory, and self-awareness, and this network is active during activities involving memory encoding and retrieval.4747 Hajebrahimi F, Velioglu HA, Bayraktaroglu Z, Helvaci Yilmaz N, Hanoglu L. Clinical evaluation and resting state fMRI analysis of virtual reality based training in Parkinson’s disease through a randomized controlled trial. Sci Rep 2022;12(01):8024. Doi: 10.1038/s41598-022-12061-3
https://doi.org/10.1038/s41598-022-12061...
Cognition plays an important role in postural control and may interfere with gait and posture assessment and treatment.7171 Souza CO, Voos MC, Barbosa AF, et al. Relationship Between Posturography, Clinical Balance and Executive Function in Parkinson’s Disease. J Mot Behav 2019;51(02):212–221. Doi: 10.1080/00222895.2018.1458279
https://doi.org/10.1080/00222895.2018.14...
So, advances in artificial intelligence (AI) may promote and refine strategies for VR in PD rehabilitation. It will allow more precise interventions since gait is very complex and an excessive number of features requires robust computing power to obtain more accurate gait performance analysis.7272 Pardoel S, Kofman J, Nantel J, Lemaire ED. Wearable-Sensor-based Detection and Prediction of Freezing of Gait in Parkinson’s Disease: A Review. Sensors (Basel) 2019;19(23):5141. Doi: 10.3390/s19235141
https://doi.org/10.3390/s19235141...
This analysis could help detect the onset of walking abnormalities, revealing the transition from normal to pathological gait.

Besides AI will offer better resolutions of patients' data, and identify parameter changes and PD symptoms and severity, which may be shared across healthcare networks and members of the interdisciplinary team, offering more personalized treatment.1515 Ellis TD, Earhart GM. Digital Therapeutics in Parkinson’s Disease: Practical Applications and Future Potential. J Parkinsons Dis 2021; 11(s1):S95–S101. Doi: 10.3233/JPD-202407
https://doi.org/10.3233/JPD-202407...
PD rehabilitation could benefit in near future from a more effective approach with more challenged and realistic virtual environment.5252 Kwon SH, Park JK, Koh YH. A systematic review and meta-analysis on the effect of virtual reality-based rehabilitation for people with Parkinson’s disease. J Neuroeng Rehabil 2023;20(01):94. Doi: 10.1186/s12984-023-01219-3
https://doi.org/10.1186/s12984-023-01219...
Finally, VR rehabilitation should be offered to PD patients as a supplementary approach to existing proven and safe interventions until further and more robust evidence is available.5050 Lei C, Sunzi K, Dai F, et al. Effects of virtual reality rehabilitation training on gait and balance in patients with Parkinson’s disease: A systematic review. PLoS One 2019;14(11):e0224819. Doi: 10.1371/journal.pone.0224819
https://doi.org/10.1371/journal.pone.022...
,5151 Kashif M, Ahmad A, Bandpei MAM, Farooq M, Iram H, E Fatima R. Systematic review of the application of virtual reality to improve balance, gait and motor function in patients with Parkinson’s disease. Medicine (Baltimore) 2022;101(31):e29212. Doi: 10.1097/MD.0000000000029212
https://doi.org/10.1097/MD.0000000000029...
,5353 Abd-Alrazaq A, Alhuwail D, Al-Jafar E, et al. The Effectiveness of Serious Games in Improving Memory Among Older Adults With Cognitive Impairment: Systematic Review and Meta-analysis. JMIR Serious Games 2022;10(03):e35202,5757 Navarro-Lozano F, Kiper P, Carmona-Pérez C, Rutkowski S, Pinero- Pinto E, Luque-Moreno C. Effects of Non-Immersive Virtual Reality and Video Games on Walking Speed in Parkinson Disease: A Systematic Review and Meta-Analysis. J Clin Med 2022;11(22): 6610. Doi: 10.3390/jcm11226610
https://doi.org/10.3390/jcm11226610...
Hence, large trials with good methodologic designs are necessary with a focus on comparing the efficacy of VR-based rehabilitation with conventional treatments and or new emerging technologies.

Robotics

Robotic-assisted gait training (RAGT) has been employed for PD patients as a complementary approach to conventional rehabilitation treatment.6161 Alwardat M, Etoom M. Effectiveness of robot-assisted gait training on freezing of gait in people with Parkinson disease: evidence from a literature review. J Exerc Rehabil 2019;15(02):187–192. Doi: 10.12965/jer.1836618.309
https://doi.org/10.12965/jer.1836618.309...
These AP devices support the body weight, control body sway and improve the safety profile, which may benefit balance, postural control, and gait parameters.1010 Alwardat M, Etoom M, Al Dajah S, et al. Effectiveness of robot-assisted gait training on motor impairments in people with Parkinson’s disease: a systematic review and meta-analysis. Int J Rehabil Res 2018;41(04):287–296. Doi: 10.1097/MRR.00 00000000000312
https://doi.org/10.1097/MRR.000000000000...
Repetitive locomotor training may also facilitate neuromuscular regulation, provide proprioceptive cueing effect, shift the body weight from one leg to the other, reduce muscle co-contraction, improve contraction/inhibition patterns, and strengthen lower limbs. The gait-like movement may also have a positive effect on the gait central pattern generators at the spinal level.2727 Fundarò C, Maestri R, Ferriero G, Chimento P, Taveggia G, Casale R. Self-selected speed gait training in Parkinson’s disease: robot- assisted gait training with virtual reality versus gait training on the ground. Eur J Phys Rehabil Med 2019;55(04):456–462. Doi: 10.23736/S1973-9087.18.05368-6
https://doi.org/10.23736/S1973-9087.18.0...
,2929 Capecci M, Pournajaf S, Galafate D, et al. Clinical effects of robot- assisted gait training and treadmill training for Parkinson’s disease. A randomized controlled trial. Ann Phys Rehabil Med 2019;62(05):303–312. Doi: 10.1016/j.rehab.2019.06.016
https://doi.org/10.1016/j.rehab.2019.06....

There are a variety of robots utilized for rehabilitation including exoskeletal robots equipped with treadmills and end-effector robots. Robotic treadmills, such as the Lokomat gait training system, improve gait performance,2727 Fundarò C, Maestri R, Ferriero G, Chimento P, Taveggia G, Casale R. Self-selected speed gait training in Parkinson’s disease: robot- assisted gait training with virtual reality versus gait training on the ground. Eur J Phys Rehabil Med 2019;55(04):456–462. Doi: 10.23736/S1973-9087.18.05368-6
https://doi.org/10.23736/S1973-9087.18.0...
and can also be associated with VR to increase cognitive flexibility and attention shifting, as well as in executive and visuospatial skills. Visual cueing, displaying incentive messages on a screen, and auditor feedback when training with RAGT, are resources to improve the rhythm of the gait of individuals with PD.5959 Kim H, Kim E, Yun SJ, et al. Robot-assisted gait training with auditory and visual cues in Parkinson’s disease: A randomized controlled trial. Ann Phys Rehabil Med 2022;65(03):101620. Doi: 10.1016/j.rehab.2021.101620
https://doi.org/10.1016/j.rehab.2021.101...
An automated wearable exoskeleton robot may detect the hip joint angle and provide torque to assist in hip flexion and extension facilitating gait training.6060 Kawashima N, Hasegawa K, Iijima M, et al. Efficacy of Wearable Device Gait Training on Parkinson’s Disease: A Randomized Controlled Open-label Pilot Study. Intern Med 2022;61(17): 2573–2580. Doi: 10.2169/internalmedicine.8949-21
https://doi.org/10.2169/internalmedicine...

Some studies have shown the beneficial effects of RAGT for FOG in PD. One study compared treadmill gait training with RAGT. PD patients had improvement in all the outcome measures (6-minute walk test, TUG, FOG, and QoL), but freezers experienced a better reduction in FOG with RAGT than control group training with treadmill alone.2929 Capecci M, Pournajaf S, Galafate D, et al. Clinical effects of robot- assisted gait training and treadmill training for Parkinson’s disease. A randomized controlled trial. Ann Phys Rehabil Med 2019;62(05):303–312. Doi: 10.1016/j.rehab.2019.06.016
https://doi.org/10.1016/j.rehab.2019.06....
The hypothesis mechanism suggests that repetitions of rhythmic limb movements could act as an external proprioceptive cue, by reinforcing the neuronal circuits that contribute to the lower limb movements. Another possibility is that proprioceptive cues might be the same as visual and auditory cues, so they might be involved in improving gait patterns.6161 Alwardat M, Etoom M. Effectiveness of robot-assisted gait training on freezing of gait in people with Parkinson disease: evidence from a literature review. J Exerc Rehabil 2019;15(02):187–192. Doi: 10.12965/jer.1836618.309
https://doi.org/10.12965/jer.1836618.309...
Fall may also be prevented by body weightlifting wearable snuggling nursing robot. It has been shown that such a device may aid PD patients' gait performance during TUG test and offer a good level of security in preventing falls.6262 Fujii C, Wakizaka N, Araki Y, Tashiro K, Endou M. Video analysis ofsafety and reproducibility issues with the timed up-and-go test applied to patients with Parkinson’s disease. Disabil Rehabil Assist Technol 2022; 17(07):801–806. Doi: 10.1080/17483107.2020.1817990
https://doi.org/10.1080/17483107.2020.18...

There is growing evidence suggesting that the utilization of these computerized technologies could potentially transform conventional therapies by facilitating safety and real-time assessments of PD patients.7373 Mekki M, Delgado AD, Fry A, Putrino D, Huang V. Robotic Rehabilitation and Spinal Cord Injury: a Narrative Review. Neurotherapeutics 2018;15(03):604–617. Doi: 10.1007/s13311-018-0642-3
https://doi.org/10.1007/s13311-018-0642-...
This finding was confirmed by a meta-analysis study, however, RAGT does not impact on the gait velocity or walking distance of patients with PD.7474 Yang Y, Wang G, Zhang S, et al. Efficacy and evaluation of therapeutic exercises on adults with Parkinson’s disease: a systematic review and network meta-analysis. BMC Geriatr 2022;22 (01):813. Doi: 10.1186/s12877-022-03510-9
https://doi.org/10.1186/s12877-022-03510...
RAGT may also benefit PD patients' gait endurance.2424 Gryfe P, Sexton A, McGibbon CA. Using gait robotics to improve symptoms of Parkinson’s disease: an open-label, pilot randomized controlled trial. Eur J Phys Rehabil Med 2022;58(05): 723–737. Doi: 10.23736/S1973-9087.22.07549-9
https://doi.org/10.23736/S1973-9087.22.0...
Therefore, assistant robotic device training can improve gait parameters with reduced motor workload in PD patients,3434 Mate KKV, Abou-Sharkh A, Mansoubi M, et al. Evidence for the Efficacy of Commercially Available Wearable Biofeedback Gait Devices: Consumer-Centered Review. JMIR Rehabil Assist Technol 2023;10:e40680. Doi: 10.2196/40680
https://doi.org/10.2196/40680...
but more studies should be done to confirm these findings.

Summary of evidence

This review aimed to identify and synthesize key trends in AT. New technologies may be used for assistance, diagnosis, monitoring, prediction of treatment response, and assistance with therapy or rehabilitation in PD patients' gait. Although many AP resources are available, only few are actually implemented in daily clinical practice. We found some hindrances to the limited use of AT and awareness of these factors may lessen the barriers between the fast-developing technological devices and consumers, making them more accessible and also broadening their implementation in PD patients' daily living or treatment.

Besides technological issues, a lack of motivation to use WSD monitoring systems is an aspect someone also must be observant of. Patients' empowerment, gaining knowledge about new AT devices, and their participation as active players in the development of research activities may also favorably increase their adherence. In addition, usability and familiarity with new devices contribute to high satisfaction of using technology in people with PD. Tailoring the best device for each individual, greater patients' gait characterization, more patient engagement and self-assessment are details to be always reminded of when selecting AP for patients' rehabilitation.

Finally, research is needed to explore the real role of AP in PD. We also need to better ascertain which technology resource will be more appropriate for gait assessment in PD. We hope his review may inspire further research, foster innovation, and to help readers to prescribe more effective and personalized technological interventions for individuals living with PD.

Key points

  • Although AT is a valuable tool for PD management, it is not widely implemented in daily clinical practice.

  • Understanding of emerging technology is important and facilitates the recognition of the potential and utility of new AP for assessing and improving gait in PD.

  • Patient empowerment and their inclusion as active players in the development of research activities may favorably impact compliance.

  • Enjoyable, cheaper, safer, easier to use, and friendly devices may contribute to adherence to using technology.

Limitations

Limitations for this review include missed original literature on technology and gait assessment, despite our best efforts to search for relevant articles and sources derived from our references. We hoped to provide a scope description of all original research on AT and gait however, we did not conduct a formal quality assessment of included studies and our findings could be influenced by publication bias.

In conclusion, this review provided a comprehensive synthesis of the current evidence and limitations of assisted technology in managing PD gait impairments. Assisted Technology in PD gait aspires to be a valuable resource for advancing our understanding of how technology can improve the lives of PD patients since this is a rapidly evolving field with an increasing number of publications in recent years. With the understanding of the potential of such devices and the existing research landscape, we hope to guide future investigations and inspire further research, innovation, and the development of more effective and personalized interventions for individuals living with PD.

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Publication Dates

  • Publication in this collection
    28 June 2024
  • Date of issue
    2024

History

  • Received
    20 Sept 2023
  • Reviewed
    19 Nov 2023
  • Accepted
    21 Nov 2023
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