Multisensory Stimulation in Amyotrophic Lateral Sclerosis Disease: Case Report of an Innovative Proposal through Immersive Virtual Reality

Abstract

Physical–cognitive stimulation has emerged as a promising strategy for improving the quality of life of patients with amyotrophic lateral sclerosis (ALS). This case study reports on the use of immersive virtual reality (IVR) as a tool for multisensory stimulation in a woman with ALS (76 years old; 11 years since diagnosis; stage 2). The program consisted of IVR stimulation sessions (three sessions per week for 12 weeks). The results showed that the implementation of the program was feasible and safe (no adverse symptoms on the Simulator Sickness Questionnaire), as well as easy to execute (>80% on the System Usability Scale). Additionally, the participant reported improvements in aspects related to her mental health (44% depression and 20% anxiety) and improvements in her quality of life, and she also maintained her values in her functional capacity. This study presents novel and important findings by demonstrating the feasibility of implementing physical–cognitive stimulation programs with IVR in a person with ALS, allowing for multisensory stimulation with commercially available hardware and software and the generation of benefits in their health-related quality of life and mental health.

1. Introduction

Amyotrophic lateral sclerosis (ALS) is a progressive neurodegenerative disease that affects the upper and lower motor neurons, which are the nerve cells responsible for controlling voluntary muscle movement. ALS progresses with muscle weakness and atrophy, leading to a progressive lack in mobility. Patients in more advanced stages also experience difficulties speaking, swallowing, and breathing, as the muscles required for these functions are also affected. ALS is currently considered to have a multifactorial origin, deriving from a combination of genetic, environmental, and lifestyle elements. ALS is a disease with no cure at present and the available treatments are aimed at controlling the main symptoms and improving quality of life [1,2]. Amyotrophic lateral sclerosis (ALS) primarily affects the upper and lower motor neurons. Upper motor neurons are located in the brain and send signals to lower motor neurons in the spinal cord, which then transmit these signals to the muscles. When both types of neurons degenerate, muscles do not receive the appropriate signals to generate movement, leading to weakness and eventual muscle atrophy. The cause of ALS is still unknown in most cases, although around 10% of cases are hereditary. The disease typically manifests in two different ways at its onset: spinal onset with weakness in the limbs (65%) and bulbar onset with dysphonia and dysphagia (33%) [3].

Physical–cognitive stimulation has emerged as a promising strategy for improving the quality of life of patients with ALS. This approach combines physical exercises with cognitive activities to stimulate both the body and the mind, offering benefits that may help mitigate some effects of the disease [4]. The combined benefits include (1) an improvements in the quality of life: keeping both the body and mind active can lead to a greater sense of well-being and autonomy; (2) a reduction in stress and anxiety: physical and cognitive activities can act as positive distractions, reducing the emotional burden of the disease; and (3) the enhancement of neuroplasticity: cognitive activities can help maintain brain plasticity, which may positively impact the brain’s adaptation to neuronal degeneration [5,6,7].

Virtual reality (VR) technology has significantly advanced in recent years, offering new opportunities for the rehabilitation and treatment of various health conditions, including ALS [8,9]. The combination of VR with physical–cognitive stimulation represents an innovative strategy for improving the quality of life of patients with ALS [10] and other neurodegenerative diseases, such as Parkinson’s disease [11,12] and multiple sclerosis [13,14,15].

Immersive virtual reality (IVR) refers to a computer-generated environment that simulates a realistic three-dimensional experience. Using devices such as virtual reality headsets and motion controllers, users can interact with virtual environments in an immersive manner. This technology offers several benefits for rehabilitation, such as the customization of therapeutic environments and the ability to perform exercises in a safe and controlled manner [11]. The combination of IVR with physical–cognitive stimulation offers a comprehensive approach to managing ALS and other neurogenerative diseases [13,14,15,16,17,18,19], potentially generating the following benefits: (1) a holistic approach, as IVR integrates physical and cognitive exercises into a single environment, providing a more complete and efficient therapeutic experience; (2) personalization, as IVR programs can be tailored to the specific needs of each patient, adjusting the difficulty and intensity of the exercises based on individual progress; (3) accessibility and safety, as IVR provides a safe environment where patients can perform exercises and cognitive activities without the risk of injury, which is particularly important for patients with limited mobility; (4) immediate feedback, as real-time feedback allows patients and therapists to adjust exercises immediately, optimizing the rehabilitation process; (5) improvement of the quality of life, as by keeping both the body and mind active, patients may experience a greater sense of well-being and autonomy; (6) the reduction of stress and anxiety, as physical and cognitive activities can act as positive distractions, reducing the emotional burden of the disease; and (7) the enhancement of neuroplasticity, as cognitive activities may help maintain brain plasticity, positively impacting the brain’s adaptation to neuronal degeneration.

While considering all the potential positive effects that can be generated in patients with ALS by physical–cognitive stimulation carried out by means of IVR, and given the lack of evidence of its application with this group, this case study is presented. The study aims to investigate and document the benefits and challenges associated with the use of immersive virtual reality in combination with physical–cognitive exercises in the rehabilitation and management of ALS patients.

2. Materials and Methods

2.1. Patient

A 76-year-old physically inactive woman (Minimental State Examination 30 pts, Barthel Index 0 pts, 11 years with ALS diagnosis—Stage 2, height 161.5 cm, body mass 71.7 kg, BMI 27.5 kg/m²) was recruited from the Fundación San Rosendo center. The patient has other conditions, including osteoporosis, cholelithiasis, and hepatic steatosis. During the IVR training intervention, the patient was under a daily prescription of Fosavance 75 mg, Riluzol 100 mg, Bisacodyl 5 mg, Ideos Unidia 100 g, Flatoril 150 mg, Tryptizol 225 mg, Movicol 46 mg, NM Protein 10 g, and Isosource Energy 250 mL (Nutrition).

Both the significant number of years since the diagnosis and the advanced state of the pathology, in addition to a usually sedentary attitude, determine a very poor initial physical/motor condition, corroborated by a situation of great dependency to perform the activities of daily living.

2.2. Study Design

All the assessments were performed both before and after the intervention period, as shown in the flow chart of the experimental design (Figure 1). The study was conducted following the ethical principles for medical research on human subjects according to the Declaration of Helsinki and complied with all the provisions established in the Organic Law 3/2018 concerning Personal Data Protection and Guarantee of Digital Rights (Organic Law 3/2018, of May 25). According to this law, strict confidentiality of the data and the results of the tests performed must be maintained. The participant and her family were informed about the benefits and risks of the research before signing the written informed consent. Additionally, written informed consent was obtained from the subject for the publication of this case report.

2.3. Physical–Cognitive Stimulation Program

The physical–cognitive stimulation program was carried out in a nursing home. The duration of the intervention was 12 weeks, with a frequency of three alternate days per week (Monday, Wednesday, and Friday). Each session lasted 10 min, except during the first week (familiarization week), when sessions lasted 7 min. The IVR stimulation program used the HMD (head-mounted display) Meta Quest II hardware and the Alcove software (version 1.300 and available in the library at www.oculus.com accessed on 25 June 2024). The sessions involved viewing videos of iconic locations in cities worldwide and interacting with them through small movements of the neck, distal phalanges of the fingers, and also with eye movements (Figure 2).

All the exercise sessions were administered by certified exercise instructors (physical education professionals or physical therapists) who are experts in using IVR in geriatric settings. The intervention was always supervised by physicians (geriatric specialists). The seated position was chosen to accommodate the participant’s current conditions (adapted wheelchair). At the end of each session, any existence of discomfort relating to immersive virtual environment exposure was inquired about, using the Simulator Sickness Questionnaire (SSQ) [20] in its Spanish language translated and adapted version [21]. On some occasions, direct communication with the participant became complicated, requiring the use of pictograms.

2.4. Assessment

Two moments (T0–T1) were established for the assessment (pre–post).

2.5. Functional Capacity

The participant’s functional impairment was assessed using the Spanish-adapted ALS Functional Rating Scale-Revised (ALSFRS-R). This validated and widely used diagnostic tool measures fine and gross motor skills in the arms and legs, bulbar function, and respiratory abilities. The scale consists of 12 concise questions, each with 5 response options ranging from 0 to 4, giving a total score between 0 and 48 points. Lower scores indicate greater functional impairment and more severe disease progression. The monthly decline in ALSFRS-R score, or delta ALSFRS-R, reflects the rate of deterioration and serves as a predictor of survival [22].

2.6. Hospital Anxiety and Depression Scale (HADS)

The Hospital Anxiety and Depression Scale (HADS) is a 14-item self-report screening tool originally designed to identify potential anxiety and depression in patients within a non-psychiatric medical outpatient setting. The scale is divided into two subscales, each containing 7 items: one for anxiety and one for depression. Each item is rated on a 4-point Likert scale (e.g., “as much as I always do” (0), “not quite so much” (1), “definitely not so much” (2), and “not at all” (3)), with each subscale yielding a maximum score of 21. The questionnaire assesses symptoms experienced over the previous week. For this study, we used the version of HADS validated by Herrero et al. [23].

2.7. Quality of Life

The EQ-5D is a general questionnaire designed to assess health-related quality of life. It evaluates health status by measuring patients’ perceptions of their functioning across five dimensions: mobility, self-care, usual activities, pain/discomfort, and anxiety/depression. The scores from these five dimensions are combined into a single “health utility” score, ranging from 1 (indicating perfect health) to 0 (indicating poor health). Additionally, a visual analogue scale (VAS) is used to rate overall health [24].

In addition to evaluating the previously mentioned aspects, parameters related to IVR exposure were assessed in order to determine the possible existence of cybersickness by using the SSQ [20,21] and those relating to the ease of use of the hardware and software by using the System Usability Scale (SUS) [25].

3. Results

Regarding the feasibility and usability of the proposed program, no clinical complications were observed during the exercise protocols. The patient did not report any discomfort or pain while carrying out the IVR program (no SSQ symptoms were reported). SUS was high (>80%). All the planned exercise sessions were completed by the patient with 100% adherence. These results suggest that the use of IVR could be safe, tolerable, and easy to manage in people with ALS, as no adverse symptoms were presented during or after the use of this technology.

It should be noted that the patient’s relationship with the center’s rehabilitation tasks was difficult. She had recently refused to go to the therapy area, showing some nervousness and anxiety. When the possibility of applying different therapy with another person as a guide that could be developed in virtual settings was raised, it had the approval of the participant from the first moment, with good reception in terms of initial motivation and better mood.

Table 1. Assessment and differences between pre- and post-intervention in body composition, functional capacity, anxiety and depression and quality of life in a 76-year-old ALS patient.

Variable	Pre (T0)	Post (T1)	Δ %
Body composition
Height (cm)	161.5	161.5	-
Body mass (kg)	71.7	69.8	2.64
Body mass index (kg/m2)	27.5	26.76	2.69
Functional capacity
ALSFRS-R	10	10	-
Anxiety and depression			-
HADS–Depression	9	5	44.44
HADS–Anxiety	10	8	20.00
Health-related quality of life
Mobility	4	4	-
Self-care	4	4	-
Usual activities	4	4	-
Pain/discomfort	3	2	33.33
Anxiety/depression	3	2	33.33
Visual analogue scale	50	65	30.00

presents the results obtained at the two evaluation moments following the performance of the multisensory stimulation program for ALS, as well as the percentage of improvement achieved by the patient. The main results indicate that after carrying out the proposed program, the participant experienced a slight change in body composition (reduction in body mass (2.64%) and body mass index (2.69%)). Functional capacity maintained its values. However, the parameters that improved the most were related to mental health: depression (44.44%) and anxiety (20.00%). The analysis of the quality-of-life data related to health perception also reported an overall improvement of 30.00% (visual health scale) while the domains for pain/discomfort, and anxiety/depression, were 33.33% and 33.33%, respectively.

4. Discussion

This case report explored the uses of IVR as a strategy for physical–cognitive stimulation in a woman diagnosed with ALS. The main results showed that this proposal is feasible and safe for people with this condition and was able to generate positive results in the parameters of body composition, anxiety/depression, health-related quality of life [26], and in maintaining functional capacity values (ALSFRS-R). ALS is typically characterized by a rapid disease course, progressing from normal functioning to one requiring assistance with basic functions, then advancing to significant disability, and ultimately leading to death. ALS has a substantial negative impact on patients’ quality of life across multiple domains, such as mobility, self-care, emotional functioning, activity impairment, and fatigue.

The use of this technology in people with major functional limitations has not prevented the development of the therapy from being safe, without adverse effects linked to virtual exposure (no SSQ symptoms), and with high levels of usability (>80%). These findings are in line with studies that assessed these aspects in people with advanced PD, who, like our participant, also required a wheelchair to get around [27]. On the other hand, other research with IVR in patients with multiple sclerosis has shown that there are no serious adverse effects and that adherence to treatment increases [28,29].

Our results have demonstrated that the use of multisensory stimulation programs carried out with IVR, despite being tested on a patient with an advanced case of the disease, can contribute to an improvement in health-related quality of life, primarily in the pain/discomfort and anxiety/depression parameters. Similar results were found by authors such as Meng et al. [30] and Tsitkanou et al. [31] when implementing physical stimulation programs (exercise-based programs) in this group, although without having used IVR.

Chipika et al. [32] confirmed that there is involvement of sensory circuits in ALS, so in addition to obvious motor impairment, somatosensory, auditory and visual pathways can cause significant clinical symptoms. Thus, the use of multisensory therapies is essential for improving the functionality and quality of life of ALS patients. Other studies, such as that performed by Trevizan et al. [9], have highlighted that devices promoting patients’ interaction with computer-based tasks can enhance their performance, leading to greater independence and the use of technology in ALS. High-tech devices such as eye tracking communication devices are used to aid communication in the later stages of ALS [33]. In our case, this same technology has also helped to carry out therapy. Initially, as is usual in the handling of these devices, the patient began to use the controls, taking advantage of the movement she had in her distal phalanges. Seeing in the first sessions that, for the correct development of the intervention, it had to have the continuous support of the attending therapist, the program was managed through head and eye movements. Although an objective assessment of cervical ROM was not performed, using the RVI program in this way led to an improvement in neck mobility, both in flexion–extension, and in rotations and lateral inclinations. This positive subjective evaluation was observed, not only by the patient’s therapists and caregivers, but also by the patient herself. Possibly, this could be an underlying reason for the adherence to the treatment that occurred, in addition to the motivation that this type of interventions usually entails in patients.

On the other hand, no changes were observed in the patient’s perception of autonomy due to the advanced stage of the disease and the degree of involvement of this particular case. However, care staff reported a positive change in their mood and increased collaboration with tasks in basic activities of daily living within their large limitations.

In addition, the nursing assistants noticed that the patient was more awake and cheerful in the mornings, asking on therapy days if the person supervising the intervention was already at the center.

In our case, the use of a commercially available HMD device (Meta Quest 2) could be rolled out to other patients with this and other chronic neurodegenerative diseases. There are examples of its use for people with Parkinson’s disease as an exercise facilitator [12], and as a therapeutic and diagnostic tool in several neurological conditions [34,35,36]. Furthermore, the portable nature of HMD devices could also represent an advantage for their implementation in community settings, patient associations, or home environments, similar to recent applications in pediatric oncology [37]. This device also allows operation without controllers (through the representation of the participant’s own hands in virtual environments or by directing experiences with head movements). These possibilities likely contributed to the high usability demonstrated in our case. The level of improvement obtained could be expected given the patient’s affected condition, as well as what is found in other advanced neurological conditions [29]. However, other studies where more demanding physical tasks have been implemented, based on boxing [38], rowing [39] or forced cycling [12] aimed at patients with PD, have achieved a greater impact on the physical and functional capabilities of the participants. Future studies should consider bringing this type of intervention to ALS patients if their initial abilities allow it in order to be eligible for possible improvements in their autonomy and functionality.

This study presents promising results and appears to be easily implementable. To the best of our knowledge, this is the first investigation seeking to apply multisensory therapies with IVR in ALS. However, due to the study design, these results cannot be generalized for the general ALS population. Additionally, in this case, the participant’s disease stage is uncommon, involving challenges with direct communication and difficulties in selecting virtual activities due to her difficulties with using her hands. There are certain limitations related to physical improvements, since changes in body composition and mobility indices cannot be associated with the implementation of the technique. Additionally, maybe the opinion of the authors and their perspective can introduce a bias that hinders the understanding the results. Despite these limitations, this study opens the door to future interventions in this field, using this technology and these virtual programs.

Future Directions

In view of what is described in this case study, future research aimed at patients with advanced ALS should include physical evaluations of mobility and joint ranges or respiratory capacities. From a neurological point of view, the possibility of incorporating imaging tests (MRI or brain CT) could identify possible changes at this level. Additionally, performing sleep quality tests or stress measurements through salivary cortisol levels would complete the information obtained through questionnaires and scales. Finally, the incorporation of smart bands or watches could make it easier to know sleep patterns and the level of weekly physical activity, and monitor parameters, such as heart rate or blood pressure.

5. Conclusions

This study presents novel and important findings by demonstrating the feasibility of implementing physical–cognitive stimulation programs with IVR in a person with ALS, allowing multisensory stimulation with commercially available hardware and software, and generating benefits in their health-related quality of life and mental health. Future research with higher methodological quality studies is necessary to confirm the findings shown in this case study.