Role of virtual reality in examining the effect of fear of falling (FOF) on postural stability in individuals without and with Parkinson’s disease in Egypt: a mixed-methods feasibility study protocol

Abstract

Background

Falls are common in older people and individuals with neurological conditions. Parkinson’s disease (PD) is known for postural instability causing mobility disabilities, falls and reduced quality of life. The fear of falling (FOF), a natural response to unstable balance, can worsen postural control problems. Evaluating FOF relies largely on affected persons’ subjective accounts due to limited objective assessment methods available. The aim of this mixed-methods feasibility study is to develop an assessment method for FOF while in motion and walking within virtual environments. This study will assess a range of FOF-related responses, including cognitive factors, neuromuscular response and postural stability.

Methods and analysis

This feasibility study will consist of four phases: the first two phases will include people without PD, while the other two will include people diagnosed with PD. Participants will be assessed for direct and indirect responses to real life, as well as virtual environment walking scenarios that may induce FOF. Data from questionnaires, different neurophysiological assessments, movement and gait parameters, alongside evaluations of usability and acceptability, will be collected. Semistructured interviews involving both participants and research assistants shall take place to elicit their experiences throughout different phases of the assessments undertaken. Demographic data, the scores of assessment scales, as well as feasibility, usability and acceptability of the measurement methods, will be illustrated via descriptive statistics. Movement and gait outcomes, together with neurophysiological data, will be extracted and calculated. Exploring relationships between different factors in the study will be achieved using a regression model. Thematic analysis will be the approach used to manage qualitative data.

Ethics and dissemination

This feasibility study was approved by the Ethics Committee of the Faculty of Physical Therapy, Kafr El Sheikh University, Egypt (number: P.T/NEUR/3/2023/46). The results of this study will be published in a peer-reviewed journal.

Trial registration number

ClinicalTrials.gov Registry (NCT05931692).

STRENGTHS AND LIMITATIONS OF THIS STUDY.

• This mixed-methods feasibility study presents a comprehensive analysis of multiple body systems response to fear of falling, which can help provide an objective measure for falling concerns.

• Using synchronised multiple equipment to track different body responses to fear of falling promotes the accuracy of measures.

• Introducing real-life fearful events through fully immersive virtual reality experience facilitates an ‘on time’ detection of fear of falling.

• Difficulties in including participants with diverse characteristics, such as age range and sex, might be an expected limitation in this study due to factors related to culture, setting and study procedures.

• The study involves only participants with Parkinson’s disease who can walk independently without aids, which may limit the ability to generalise the study results to a less functioning population with Parkinson’s disease.

Background

Falls represent a major cause of injury, posing heightened risks among individuals aged over 60 years,¹ and those with chronic neurological conditions.^2–4 In 2021, the WHO reported an annual global toll of nearly 685 000 fatalities resulting from falls, with over 80% concentrated in low and middle-income countries.¹ Postural instability is considered a prominent manifestation in Parkinson’s disease (PD), and it becomes more disabling with progression of the disease.⁵ The disturbance of balance control mechanisms may contribute to falling, impacting gait parameters and restricting mobility, ultimately resulting in functional dependency.⁶ Frequent occurrences of falls are noted in individuals with PD⁷; it is reported that the rate of falls in people with PD is considered one of the highest among other chronic neurological disorders, with an estimate of 77% of those with PD fall every year.⁸ In most cases, community-based falls occur at least once due to environmental factors such as cluttered or busy areas and challenging terrains that require high attentional demands and quick reactions.⁹

The interaction between postural control and emotional responses has been increasingly highlighted over the last two decades.^10–21 Fear of falling (FOF) is one of the emotional reactions that are quite common in older adults,^{20 22 23} and even more prevalent in persons diagnosed with conditions that disturb the balance system, such as PD.^24–26 Fear of falling may affect postural control in older adults¹⁶; a considerable number of studies have found an elevation in frequency and reduction in amplitude of the centre of pressure (COP) under fearful situations.13 15 27–29 In a study by Maki et al,²⁰ a greater displacement of COP was noticed in older adults who showed self-perceived FOF compared with their peers who did not have falling concerns. When it comes to people with PD, the situation may get even worse; excessive and unjustified FOF, which may develop especially after experiencing the first fall, contributes to further deterioration of balance which is already disrupted by the disease.^30–33 This can lead to avoidance of many physical activities and exaggeration of symptoms, consequently affecting the overall quality of life.³⁴

Neuroimaging studies of anxiety disorders have revealed that patients with anxiety and excessive fear exhibit functional and structural abnormalities within the prefrontal–amygdalar neural fear circuit, highlighting the role of the prefrontal cortex (PFC) in pathological inhibition of fear and cognitive reappraisal of emotions.³⁵ Patients with anxiety and FOF demonstrate hypoactivation in the PFC, inversely correlated with hyperactivation in the amygdala.^{36 37}

FOF is multidimensional in nature, encompassing various underlying constructs, such as fall-related concerns and fall efficacy, each requiring distinct measurement approaches.³⁸ For this reason, the generalisation of results from studies using measurements of different constructs is quite complicated.³⁹ Moreover, fall-related concerns are usually assessed through subjective self-perceived questionnaires,^{40 41} introducing the likelihood of systematic bias in results.⁴² Falls Efficacy Scale (FES) and Activities-Specific Balance Confidence Scale (ABC Scale) are the most widely used measures in clinical and research settings, as they rely primarily on the person’s own evaluation and perception of fear and self-efficacy during diverse activities and conditions.⁴⁰

Electrophysiological assessment is a highly objective and reliable method of measuring different neural and neuromuscular activities. Electroencephalography (EEG) is one of the electrophysiological examination methods with considerable reliability that has been widely used for direct detection of different emotions and psychological states including fear and anxiety.^43–45 In addition, electromyography (EMG) is an excellent tool of measuring spontaneous reaction of muscles to fear.^{46 47} Fear can also be detected indirectly through examination of fear-related body responses, such as changes in heart rate^48–50 and postural adjustments.13 15 27–29 51

Virtual reality (VR) is computer-based software that provides an enjoyable and interactive environment and helps promote physical and psychological activity engagements.⁵² Virtual environments can be specially designed to serve the purpose of use and suit different population categories. It can help revisualise situations that evoke FOF and mobility concerns in a controllable manner.⁴³ Recently, VR has been used in physical rehabilitation and as a tool for exposure therapy in people who experience different types of phobias, such as arachnophobia. However, exploring the ability of VR to help assess psychosomatic symptoms such as FOF has not yet received adequate attention.

Developing objective assessment protocol for FOF can eliminate the bias in self-report and overcome other limitations. Real-time, synchronised, movement-based and objective physiological assessments of movement-related concerns are lacking.^{53 54} Most of the studies that were aiming to develop an objective measuring strategy for FOF with the help of VR to induce fear had different experimental setups, evaluated FOF during static positions (eg, sitting and standing)27 39 54 55 and were applied on population who do not have pathological conditions that might be disabling.27 39 54 55

In order to explore the efficacy of any intervention that targets controlling excessive FOF during physical rehabilitation in general, and neurological rehabilitation in particular, it was important to develop an objective measurement of such self-perceived and psychological experience. We consider this study a first step towards creating a feasible, objective, cost-effective and acceptable measure of FOF that allows for transition of the resulted refined measurement strategy outside laboratories and research settings. Thus, this study is aiming to: (1) develop a synchronised, accurate and robust assessment protocol for different responses of the neuromuscular system to FOF and postural instability (this will be implemented during body movement and walking in challenging environments that mimic real-life scenarios through VR system); (2) explore feasibility, acceptability, safety and usability of this method; and (3) evaluate the feedback and opinions of participants and research assistants during the application of instruments and conduction of assessment procedure through semistructured interviews and focus groups.

Methods and analysis

Study design

This is a multiphase, sequential, mixed-methods feasibility study that will be conducted through evaluation of FOF and balance performance in people without and with PD. The study will consist of four phases: phase I, a feasibility study will be conducted on participants not having PD, and data will be collected from neurophysiological measurements, movement and gait assessment, and questionnaires; phase II, where semistructured interviews will be conducted for participants involved in phase I, whereas focus group will be held for the research assistants; phase III, in which according to the outcomes of phases I and II, necessary modulations in the assessment protocol may take place, if needed, in order to be applied to people with PD during this phase; and phase IV, where phase II will be repeated; however, people with PD will be interviewed instead. Data collection is expected to begin in July 2024 and to be completed by the end of 2025.

Setting

The study will be conducted at Human Mechatronics Lab, Ain Shams Virtual Hospital, Ain Shams University, Cairo, Egypt.

Participants

Two groups of participants, who are aged 40 years or older, will be involved in this study. Each group will have from 10 to 30 participants. The first group will include a group of people without PD and the second group will include people with PD, both will be screened for eligibility. Participants who meet the inclusion criteria will go through the planned assessment procedure.

Inclusion criteria

Group I

• Individuals aged ≥40 years old.

• People without musculoskeletal or neuromuscular conditions.

• People who are not experiencing any type of pain at the time of examination procedure.

Group 2

• Individuals aged ≥40 years old.

• Participants diagnosed with PD by a neurologist, regardless of the type.

• Modified Hoehn and Yahr stages I–III.

• Able to follow instructions and understand questions.

• Able to walk independently and without walking aids.

• People who experience excessive FOF and fear of movement.

• Able to communicate verbally.

• Stable use of PD or other comorbidities medications.

Exclusion criteria

• Severely impaired vision and hearing.

• Unstable medical condition.

• Coexisting neurological or orthopaedic conditions that may limit mobility and affect participation.

• Dizziness, vertigo, headache and motion-sickness.

• Severe cognitive impairment.

• Pregnancy.

Procedure

Phases I (people without PD) and III (people with PD)

After recruiting participants, screening them for eligibility and having their signed consent, the assessment procedure shall begin. Assessments will be performed ensuring that participants have not engaged in strenuous activity or consumed coffee/tea or food in the previous 2 hours. The assessment procedures will include demographic data collection, movement outcomes, neurophysiological outcomes, questionnaires, physical activity and safety, usability and acceptability.

• Demographic data will be collected including age, sex, diagnosis, symptoms severity measured through Movement Disorder Society-sponsored Unified Parkinson’s Disease Rating Scale (MDS-UPDRS), occupation, medication, medical history.

• Assessment procedure will be performed at the same time of day with participants who have PD taking medication as normal. The assessment of movement, gait and neurophysiological outcomes will take place during implementation of a movement scenario within both virtual and real environments (with and without VR system).

• The following assessment procedures will be conducted:

Step 1 (secondary outcomes)

• Fear of falling will be assessed using Falls Efficacy Scale International (FES-I).

• Balance confidence, using Activity-specific Balance Confidence scale (ABC Scale).

• Balance and functional mobility, through Mini Balance Evaluation Systems Test (Mini-BESTest).

• Cognition, using the Montreal Cognitive Assessment (MoCA).

• Depression and anxiety, using Hamilton Depression and Hamilton Anxiety Rating Scales (HAM-D and HAM-A).

• Participation using WHO Disability Assessment Schedule (WHODAS).

• Health-related quality of life will be evaluated by Parkinson’s Disease Questionnaire 39 (PDQ-39).

Step 2 (primary outcomes)

A movement scenario composed of standard validated functional tasks will be created, including sit to stand, walking, turning, reaching and moving over an obstacle, under normal (real laboratory environment) and distracting conditions (virtual environment). During the execution of this movement scenario, postural response, gait and neurophysiological outcomes will be measured.

The virtual environment: FOF will be induced through a head-mounted display (Meta Quest 3) which consists of a VR headset, a pair of body-mounted controllers and a positioning-system tracking display in order to move into a virtual environment. The environment will be specially designed and created to simulate real-life scenes that evoke fear in people with PD, such as crowds, stairs, doorways and narrow corridors.

Postural response and gait outcomes

Balance and movement and its control will be measured throughout the movement scenario via:

• Marker-based Qualisys motion capture system: for measuring spatiotemporal gait parameters including walking speed, stride length and joints positions.

• Force platforms: mainly for assessment of COP displacement and trajectory.

• Postural inertial measurement unit (IMU): placed over the projected centre of mass located over the fourth lumbar vertebra. The IMU sensor includes triaxial gyroscope, magnetometer and accelerometer, and will assess postural sway through measurement of the speed and orientation of tilt, body mass centre acceleration and changes in posture.

Neurophysiological outcomes

The reaction of neuromuscular system to fear will be monitored throughout the movement scenario via real-time EEG and EMG.

• EEG signals will be acquired using 64-channel EEGO sports portable EEG system and Waveguard caps (ANT Neuro, Hengelo, The Netherlands). The behaviour of EEG signals will be recorded during the performance of the designed movement scenario associated with fear-evoking situations (introduced through VR) as well as under normal conditions (without VR). Preprocessing will include filtering, re-referencing, artefact correction and rejection. Spectral analysis for the various EEG wave bands will be done. A machine learning model will be trained to classify fear versus no fear based on features extracted during the analysis.

• EMG signals will be collected using the Trigno wireless EMG system (Delsys, Natick, Massachusetts, USA). Amplitude and frequency of muscle activation signals, muscle activation timing, and co-contraction patterns and ratios between agonist/antagonist pairs will be measured and recorded through direct placement of EMG sensors over medial hamstring, rectus femoris, medial gastrocnemius and tibialis anterior of both legs for each participant.

• Polar H10 heart rate sensor will be used to monitor heart rate changes during both fear-evoking and normal situations.

Feasibility, acceptability, usability and safety

Feasibility

• Evaluating to what extent the participants can complete the study protocol as planned and proposed, and difficulties or facilitators to implementation.

• To what extent this measurement protocol is applicable and likely to be used, especially in different populations and settings.

• Cost-effectiveness and suitability with available resources.

Acceptability and usability

• The degree of satisfaction and suitability with culture.

• Suitability Evaluation Questionnaire for virtual rehabilitation systems (SEQ) will be used.⁵⁶ Effort will be recorded during the session through Borg Rating of Perceived Exertion Scale (Borg RPE).⁵⁷

• Sense of presence, using iGroup Presence Questionnaire (IPQ), which is a scale for measuring the sense of presence experienced in a virtual environment.⁵⁸

• The ability to recruit participants.

• Directly after implementation of the procedure, each participant will be given a questionnaire to report the most fearful moments/scenes, and to rate the level of FOF they experienced during these moments giving a score out of 10, where 10 indicates the highest level of fear.

Safety

• Any adverse events during the procedure including falls, dizziness or discomfort will be monitored, and any after-effects will be recorded.

Phases II (people without PD) and IV (people with PD)

These are the qualitative stages of the study, where interviewing all the participants and conducting a focus group for the research assistants will explore the perceived barriers and facilitators, including safety and applicability, to implementation of the assessment. In order to participate in the qualitative study, both participants and researchers should have been involved in the quantitative stages of the study.

The research team

The research team who will implement the qualitative research are highly qualified and professional physiotherapists and research assistants. This team will be led and guided by YSG (PhD) who has considerable experience in qualitative research methods, especially in people with chronic neurological conditions. The participants will be familiar with the team as they already communicated during phases I and III of the study.

Context

Face-to-face semistructured interviews for the participants will occur at Ain Shams University Hospital, whereas an online meeting will be arranged for the focus group.

Data collection methods

Semistructured questions will be especially tailored for the study. The interviews will be conducted privately, it should not exceed 45 min in duration and it will be audio recorded. The focus group will take place online, and the meeting will be video recorded. The data obtained through both recordings will be accurately transcribed.

Control of bias

The credibility of results will be promoted by (1) independent review of data, coding and development of themes by more than two researchers (discussions will take place until achieving consensus); (2) involving participants who only experienced phase I and/or phase III of the study; (3) precise transcription of the recorded data and checking to compare between the recordings and transcripts; (4) reporting supportive quotations by the participants for each emerging theme.

Patient and public involvement

This research has considered the participant as a crucial part in the decision-making process regarding the feasibility of the intended measurement strategy. In this study, obtaining both public and patients’ feedback after applying the designed methods, paying high attention to their perspective through interviews and focus group, will help configure the final form of a feasible assessment protocol for excessive FOF that may occur during real-life activities of people with neurological conditions, particularly PD.

Data management and statistical analysis

All data will be coded and saved securely by the project researchers. Descriptive statistics will be used to describe feasibility, usability and acceptability. All questionnaires’ scores will be presented using descriptive statistics as well.

For movement, gait and neurophysiological parameters, repeated-measures analysis of variance will be used with condition (VR vs real environment) as the within-subjects variable. Regression models will evaluate relationships between self-reported FOF, balance confidence scores and the quantified movement/neurophysiological parameters. The variables are:

• Dependent variables: COP displacement, sway measures, EEG/EMG signals.

• Independent variables: FOF and balance confidence scores.

• Covariates: age, gender, severity of symptoms, level of cognition, depression and level of functional balance.

Potential sensitivity and specificity will also be analysed to examine threshold cut-off values for VR movement parameters to distinguish excessive FOF based on the comparison with non-VR condition results, FOF and balance confidence questionnaires, and feedback from participants.

Missing data will be reported with reasons given where available and the missing data pattern will be explored.

Qualitative data will be processed through a thematic analysis approach. It will involve giving codes, categories, themes and subthemes to the transcripts, and identifying commonalities. Researchers will screen transcripts several times aiming for familiarisation, and code them independently line by line.

Ethics and dissemination

This study was approved by the Ethics Committee of the Faculty of Physical Therapy, Kafr El Sheikh University, Egypt (number: P.T/NEUR/3/2023/46).

A signed informed consent form will be obtained from the participant, next of kin or the participant’s legal guardian before data collection. Upon completion of this study, results will be published in a peer-reviewed scientific journal.

Ethics statements

Patient consent for publication

Not applicable.