Воздействие телереабилитации на физическую функцию и повседневную жизнь пациентов с амиотрофным боковым склерозом: обзор аналитического исследования.

INTRODUCTION

Amyotrophic lateral sclerosis (ALS), a progressive disease that typically develops in middle age or later, causes the degeneration of motor neurons in the cerebral cortex, brainstem, and spinal cord 1 , 2 ) . The age of onset is most commonly between 50 and 70 years, and its incidence in Japan is reported to be 2.2/100,000 persons/year, with a prevalence of 9.9/100,000 persons/year 3 ) . Symptoms generally begin with muscle weakness in the extremities, but bulbar symptoms precede limb weakness in approximately one-third of the patients 1 ) . Regardless of the initial site of onset, the disease progresses throughout the body, resulting in upper extremity dysfunction, gait disturbances, dysarthria, dysphagia, and respiratory failure 2 ) . The time from onset to death or the need for ventilatory support was 32–48 months. Riluzole and Edaravone have been approved as drug therapy in Japan 4 , 5 ) . However, although Riluzole prolongs survival by 2–3 months, it does not improve motor function 6 ) . Edaravone is only effective in patients with mild symptoms 7 ) , and the effects of disease-modifying drugs remain limited. Therefore, symptomatic treatments such as gastrostomy, ventilatory support, and rehabilitation are important for maintaining and improving activities of daily living (ADL) 1 , 2 ) .

However, evidence for rehabilitation in patients with ALS remains limited, one reason for which is the difficulty of continuing rehabilitation 2 , 8 ) . As the disease progresses, mobility becomes increasingly impaired, making it difficult for patients to undergo rehabilitation at medical institutions 9 ) . As the severity of the disease progresses, priority is given to using home nursing care and helpers, which often results in an inadequate allocation of home rehabilitation services within the healthcare insurance system. Consequently, monitoring and guidance by specialists are insufficient, and adjusting exercise methods and intensity according to symptoms is difficult, which may lead to fatigue and overuse muscle weakness due to overload, or disuse muscle weakness due to inactivity 9 ) . Decreased adherence to rehabilitation programs, such as dropouts from protocols, has been reported in patients with ALS 8 ) . Therefore, there is a need for a rehabilitation approach that enables patients with ALS to learn appropriate exercise methods at home and allows healthcare providers to manage them effectively.

Since the COVID-19 pandemic, telemedicine has spread rapidly and has been incorporated into rehabilitation. Telerehabilitation is the use of information and communication technologies such as smartphones, tablets, and personal computers to provide rehabilitation to patients in remote areas without physical contact with them 10 ) . Its advantages include eliminating the need for patients to travel to medical institutions, allowing them to review instructional content at their convenience, and enabling healthcare providers to accurately monitor patients’ conditions at home 11 ) . In neurodegenerative diseases such as Parkinson’s disease and multiple sclerosis, telerehabilitation has been shown to improve adherence, physical function, and ADL 12 , 13 ) . Online consultations and monitoring using wearable devices have started 14 ) . However, reports on telerehabilitation for patients with ALS remain limited, and although a few review articles 11 , 15 ) are available, no studies systematically have reviewed the literature.

Therefore, this study aimed to systematically map and synthesize the existing evidence on the effects of telerehabilitation on physical function and ADL in patients with ALS, with the goal of identifying current trends, challenges, and research gaps through a literature review.

PARTICIPANTS AND METHODS

In integrating the findings of previous studies on telerehabilitation in patients with ALS, we anticipated that conducting a systematic review would be difficult due to the limited number of previous high-quality studies. Recently, scoping reviews have received increasing attention. A scoping review aims to comprehensively survey the current research by mapping a wide range of literature and identifying research gaps 16 ) . Therefore, we adopted a scoping review based on the PRISMA Extension for Scoping Reviews reporting guideline 17 ) .

The PubMed, Scopus, Web of Science, and ProQuest databases were searched. The literature search was conducted until December 31, 2024, with no specific starting date. To ensure comprehensive coverage, the articles were retrieved from the earliest available records in each database. We identified search keywords and synonyms based on previous studies of neurodegenerative diseases 12 , 13 ) and formulated the following search formula:

Search formula (PubMed)

#1. “Amyotrophic lateral sclerosis”[Mesh] OR “Motor neuron disease”[Mesh]

#2. “Exercise Therapy”[Mesh] OR “Exercise”[Mesh] OR

“Physical Therapy Modalities”[Mesh] OR “Rehabilitation”[Mesh] OR

“Occupational Therapy”[Mesh] OR “Speech Therapy”[Mesh] OR

“Language Therapy”[Mesh] OR “Resistance Training”[Mesh] OR

“Endurance Training”[Mesh] OR “Breathing exercises”[Mesh] OR

“Muscle Stretching Exercises”[Mesh] OR “Patient Education as Topic”[Mesh]

#3. “Telerehabilitation”[Mesh] OR “Telemedicine”[Mesh] OR

“Videoconferencing”[Mesh] OR “telepractice” OR “tele-monitoring” OR “remote” OR

“telehealth” OR “video”

#4. #1 AND #2 AND #3

Search formula (Scopus, Web of Science, ProQuest)

#1. “amyotrophic lateral sclerosis” OR “motor neuron disease”

#2. “exercise therapy” OR “exercise” OR “physical therapy” OR “physiotherapy” OR “rehabilitation” OR “occupational therapy” OR “speech therapy” OR “language therapy” OR “resistance training” OR “endurance training” OR “breathing exercise*” OR

“muscle stretching exercise*” OR “patient education” OR “physical activity”

#3. “telerehabilitation” OR “telemedicine” OR “videoconferenc*” OR “telepractice” OR

“tele-monitoring” OR “remote” OR “telehealth” OR “video”

#4. #1 AND #2 AND #3

In addition to the database search, a manual search was conducted to ensure comprehensive identification of relevant studies. Specifically, we screened the reference lists of review articles on the rehabilitation of patients with ALS to identify additional studies that may have been missed in the initial search. The selection criteria for the literature were as follows: articles that included patients with ALS, articles that practiced telerehabilitation, and articles that used physical function and ADL as outcomes. The exclusion criteria were as follows: articles written in non-English or non-Japanese languages, conference abstracts, and articles that were difficult to obtain. Although ADL was not included as a keyword in the search formula, studies were included if they assessed either physical function or ADL as an outcome based on the eligibility criteria. Articles using telephone or e-mail in telerehabilitation were usually included; however, this study, based on the recent definition, included studies using video calls, biomonitoring, and on-demand video format and excluded those using only telephone or e-mail 10 ) . Duplicate documents identified during the database search were removed before the primary screening. Two evaluators independently evaluated the retrieved literature according to the selection criteria: by title and abstract in the primary screening, and by full text in the secondary screening. Study design, sample size, intervention type and duration, telerehabilitation methods, adherence (dropout and compliance rates), outcomes, effectiveness, adverse events, and patient satisfaction were extracted for the selected literature. We defined the dropout rate as the proportion of patients who dropped out during the intervention period, and the adherence rate as the proportion of patients who did not drop out and adhered to the protocol during the intervention period.

This study was a scoping review of existing literature and was not subject to ethical review because no new data were collected. However, all collected studies adhered to ethical standards. Care was taken to avoid copyright infringement, and data extracted from the original studies were used with proper attention to citations and source acknowledgments.

RESULTS

A flowchart of the literature selection process is shown in Fig. 1 Fig. 1. Flowchart of literature selection. . We identified 360 documents. After removing 140 duplicates, 220 documents were screened in the primary screening. After primary and secondary screening, six articles were selected. However, two papers by Braga et al. 18 , 19 ) were combined because they were doctoral dissertations and research papers submitted to a commercial journal with the same subject, intervention methods, and results. The selected articles are summarized in the review sheet ( Table 1 Table 1. Review sheet Author Design Sample size Gender (Male:Female) Type of intervention Intervention period Telerehabilitation methods Adherence Outcome Effect Year of issue Age (years) c) Country ALSFRS-R b) (points) c) Braga (2018) 18 ) Case-series study 7:3 Aerobic exercise 6 months Monitoring SpO 2, HR, METs, and step count. Dropout rate 0%. ALSFRS-R, %FVC d) , METs, SpO 2 ALSFRS-R and METs showed significant deterioration, while %FVC and SpO 2 showed no significant differences. Braga (2019) 19 a) n=10 57 ± 9.1 Compliance rate 121%. Portugal 43.0 ± 2.1 Burke (2021) 20 ) Case-series study 31:22 Stretching 4 weeks The video group received on-demand video instruction. Dropout rate 13%. VAS No significant difference. USA n=53 - Booklet group 14%. Booklet group n=28 - Video group 12%. Video group n=25 De Marchi Case-series study 7:12 Comprehensivephysical therapy 2 months Video dialogue. Dropout rate 21%. BI, VAS, BS All exacerbated. (2021) 21 ) n=19 51.5 ± 12.2 Italy 32.1 ± 9.2 Kiefer (2022) 22 ) Case-series study n=13 8:4 Expiratory muscle training 6 weeks Assessment and remote practice using Zoom. Dropout rate 8%. MEP, PEFR. MEP showed significant improvement, while no significant differences were observed in other parameters. USA 60.1 ± 8.7 Compliance rate 90%. Audio/Video analysis, Perceptual speech assessment 39.0 ± 3.8 On-demand video instruction. Vicente-Campos Case-control study - Inspiratory muscle training 8 weeks Confirmation of adherence status by phone and video conferencing. Dropout rate 0%. PImax, HR, HRV, ALSFRS-R PImax, HR, and ALSFRS-R were significantly higher, while no significant differences were observed in other parameters. (2022) 23 ) Intervention group n=10 49.6 ± 8.6 Spain Control group n=10 34.4 ± 7.8 a) The two papers by Braga et al. 18 , 19 ) were submitted as research papers and doctoral theses by the same author and their contents were identical. b) ALSFRS-R: The total score ranges from 0 to 48 points. Higher scores indicated lower severity. c) Age (years) and ALSFRS-R (points) were shown as mean ± standard deviation. d) %FVC, the percentage of expected lung capacity at which a person can exhale. ALSFRS-R: amyotrophic lateral sclerosis functional rating scale-revised; BI: Barthel index; BS: Borg scale; %FVC: % forced vital capacity; HR: heart rate; HRV: heart rate variation; M: male; SpO 2 : saturation of percutaneous oxygen; MEP: maximum expiratory pressure; METs: metabolic equivalents; PEFR: peak expiratory flow rate; PImax: maximum inspiratory pressure; VAS: visual analog scale. ).

The study designs were four case-series studies and one case-control study, all with level 4 evidence 24 ) . The publication years were 2018, 2020, and 2021 for three studies and 2022 for two studies. The included studies were conducted by Braga et al. 18 , 19 ) in Portugal, Burke et al. 20 ) and Kiefer 22 ) in the United States, De Marchi et al. 21 ) in Italy, and Vicente-Campos et al. 23 ) in Spain.

The ALS Functional Rating Scale-Revised (ALSFRS-R) 25 ) was used to determine disease severity in individuals with ALS. In previous studies, out of 48 points, 40 or more points were considered as minimal-to-mild and 30–39 points as mild-to-moderate 26 ) . Braga et al. 18 , 19 ) and Kiefer 22 ) set the case selection criteria as 30 or more points and 34 or more points, respectively, and patients with mild-to-moderate or less severity were included in their study. The other reports did not conduct case selection criteria using the ALSFRS-R, except De Marchi et al. 21 ) , who reported 32.1 ± 9.2 points (mean ± standard deviation), and Vicente-Campos et al. 23 ) , who reported 34.4 ± 7.8 points, mainly for patients with mild-to-moderate severity of disease. In a study by Burke et al. 18 , 19 ) , 74% of the participants were ambulatory. All five articles 18 , 19 , 20 , 21 , 22 , 23 ) excluded patients with cognitive impairment, and four studies included patients without respiratory assistance.

Based on the classification by O’Connell and Salsman 11 ) , the telerehabilitation methods included two cases of synchronous multi-participant conferences, one case combining synchronous multi-participant conferences with on-demand educational and training resources, one case utilizing remote equipment monitoring, and one case involving on-demand educational and training resources ( Table 2 Table 2. Telerehabilitation modalities and intervention types in included studies Author Intervention types Synchronous multi-participation conferences Remote device monitoring On-demand format education and training resources Braga (2018) 18 ) Aerobic exercise ○ Braga (2019) 19 ) Burke (2021) 20 ) Stretching ○ De Marchi (2021) 21 ) Comprehensive physical therapy ○ Kiefer (2022) 22 ) Expiratory muscle training ○ ○ Vicente-Campos (2022) 23 ) Inspiratory muscle training ○ ).

The rehabilitation intervention methods included respiratory rehabilitation in two cases and aerobic exercise, stretching, and comprehensive physical therapy in one case each. Of the reports that conducted respiratory rehabilitation, Kiefer 22 ) conducted expiratory muscle strength training for 6 weeks. The exercise method utilized an expiratory muscle training device (EMST150/EMST75 Lite, Aspire Respiratory Products) at a frequency of five times per week. Each session lasted an average of approximately 16 minutes, ranging from 6 to 27 minutes. Telerehabilitation methods included remote assessment and practice using Zoom and on-demand video instruction. Inspiratory muscle training was performed for eight weeks. The exercise method utilized an inspiratory muscle training device (POWERbreathe ® , made by POWERbreathe International), and the frequency was five times a week. Each session consisted of 30 inspirations, divided into 15 in the morning and 15 in the evening, but session duration was not reported. Braga et al. 18 , 19 ) reported six months of aerobic exercise. The exercise method included treadmill or outdoor walking, and each session lasted approximately 25 minutes, consisting of 15 minutes of walking plus a 5-minute warm-up and 5-minute cool-down. The frequency was set at least once a week, with a minimum of 24 sessions over six months. A tele-monitoring system was used to monitor transcutaneous arterial blood oxygen saturation, heart rate, and step count in real-time using a noninvasive wireless biosensor connected to a cell phone via Bluetooth. Vital sign data during the exercise sessions were immediately analyzed, and the medical team reviewed the data in real-time and adjusted the exercise protocols as needed. Burke et al. required four weeks of stretching. The participants were divided into booklet and video groups and instructed to perform the exercises as often as possible with no set frequency. Each stretching session consisted of a set of 8 to 9 exercises targeting major muscle groups, but no specific session duration was provided. De Marchi et al. 21 ) reported a multidisciplinary team that included a physical therapist who provided comprehensive physical therapy for two months, including pain management, prescription of assistive devices, and exercise instruction. The frequency was averaged three times per month, and the study was conducted during the COVID-19 pandemic entirely via video interaction. Each telehealth visit lasted approximately 20 to 30 minutes per provider, resulting in a total session time of 80 to 120 minutes. The telerehabilitation programs used in the papers in this review were all based on home exercise with remote support and monitoring. These programs differ from interventions in which physical therapists visit patients at home to provide direct exercise guidance. However, the studies by De Marchi et al. 21 ) and Vicente-Campos et al. 23 ) did include some video instruction, which is similar to home rehabilitation in some respects.

Adherence in the study by Kiefer 22 ) showed an 8% dropout rate (one patient) owing to workload. The compliance rate for the remaining participants was 90%, and Vicente-Campos et al. 23 ) reported no dropouts. Braga et al. 18 , 19 ) , who performed aerobic exercise, also reported no dropouts. Although the compliance rate was not reported, an average of 29 sessions were completed, exceeding the minimum requirement of 24 sessions over 6 months. Burke et al. 20 ) reported a 12% dropout rate and a significant increase in frequency from 4.0 to 6.0 sessions per week in the video group. De Marchi et al. 21 ) reported a dropout rate of 21% (four patients) in the comprehensive physical therapy group. Three of the four dropouts were due to telerehabilitation connection problems, and one patient died as the disease progressed.

The effects of telerehabilitation were as follows: regarding respiratory rehabilitation, Kiefer 22 ) reported improvements in maximal expiratory pressure and ALSFRS-R total score and a decrease in heart rate compared to baseline. Meanwhile, Vicente-Campos et al. 23 ) noted an increase in maximal inspiratory pressure and ALSFRS-R total score and a decrease in heart rate compared to the control group. The effect size was considered moderate or greater. Conversely, none of the patients who conducted aerobic exercise, stretching, or comprehensive physical therapy showed significant improvement compared to baseline.

Braga et al. 18 , 19 ) did not report any serious adverse events. Six of the ten patients had a maximal heart rate that was temporarily higher than expected, but the tele-monitoring system worked and corrected it quickly. Kiefer 22 ) did not describe or report any adverse events, and neither did other reports.

Kiefer 22 ) reported that patient satisfaction was high, with a satisfaction score of 4.0 out of 5, according to a Telemedicine Satisfaction Questionnaire 27 ) . The items with high satisfaction were “easy to talk to the medical provider”, “the medical provider understands my condition”, “I can hear the medical provider clearly”, “I can see the medical provider clearly”, and “it saves travel time”, while the item with low satisfaction was “telemedicine is consistent with face-to-face care”. De Marchi et al. 21 ) reported that all patients who responded to their questionnaire were satisfied with telemedicine services. The most satisfactory items were “face-to-face contact with healthcare professionals” and “the team understands my problems”, while the least satisfactory items were “ease of use of the platform” and “cost of transportation”. Burke et al. 20 ) reported that most participants found the stretching instructions easy to understand, and 61% preferred the video over the booklet.

DISCUSSION

This study used a scoping review method to investigate the effects of telerehabilitation on physical function and ADLs for patients with ALS. However, the number of selected studies was small, and they were case-control or case-series studies. Additionally, studies with a high level of evidence have not yet been reported.

Telerehabilitation methods varied across studies, including synchronous multi-participant videoconferencing, remote device monitoring, and on-demand education and training resources. Some reports used a combination of these methods. The most recent report published was in 2022. No studies have focused on the use of virtual reality, biomonitoring with smartwatches, or patient guidance using artificial intelligence, which has increased in recent years 28 ) .

Adherence was high, with dropout rates ranging from only 0 to 8%, except in the report by De Marchi 21 ) . The compliance rate was 90% in the study by Kiefer 22 ) , and although Braga et al. 18 , 19 ) did not report the specific adherence rate, a high adherence rate was maintained, with an average of 29 sessions conducted for a minimum of 24 sessions. De Marchi et al. 21 ) reported a dropout rate of 21%. Among the 21% dropout rate, three of the four dropouts were due to connection problems; only one was due to the patient’s medical condition. In a previous study, adherence to home-based rehabilitation in patients with ALS decreased because of a decline in physical function caused by disease progression, psychological problems, and time constraints. The decrease in adherence depended on the type of exercise, with most patients able to adhere to the protocol without dropping out in respiratory rehabilitation. Adherence tended to decrease slightly among patients who conducted stretching and resistance training, with a significant decline reported among those who did aerobic exercise 29 , 30 ) . Clawson et al. 30 ) reported a dropout rate of 55% after 6 months of aerobic exercise with face-to-face or telephone follow-up. Van Groenestijn et al. 31 ) reported a dropout rate of 33% and a compliance rate of 41% after 4 months of aerobic exercise and face-to-face follow-up. Patients with ASL had difficulty continuing aerobic exercise as it constitutes a whole-body exercise, which easily leads to fatigue. This is also because changing the intensity of exercise according to the symptoms is difficult 29 ) . Braga et al. 18 , 19 ) reported no dropouts, and the sessions were performed more frequently than the minimum number of sessions set after 6 months of aerobic exercise. In this study, a tele-monitoring system was used to monitor vital signs and other data in real-time. This enabled adjustment of exercise intensity according to symptoms, which is difficult in conventional home-based rehabilitation. Consequently, high adherence to aerobic exercise was maintained. Burke et al. 20 ) also reported that stretching was performed more frequently in the video group, with an average of 6.0 days per week. Although the reason for this increase was not explained in detail, the flexibility of the on-demand format, which removed time constraints, may have contributed to the increase. In conclusion, telerehabilitation effectively addressed the barriers to the continuation of rehabilitation, such as the need to adjust exercise intensity and time constraints, and enabled the patients to maintain high adherence regardless of the type of exercise.

Respiratory function, endurance, and ADL significantly improved in two reports that included respiratory rehabilitation. Although respiratory rehabilitation maintains and improves physical function and ADLs in patients with ALS 32 , 33 ) , our results suggest that respiratory rehabilitation may be effective even in telemedicine environments. Vicente-Campos et al. 23 ) reported a moderate or greater effect size. Respiratory rehabilitation does not require extensive equipment, can be easily adapted to the telemedicine environment 15 ) , and is as effective as home rehabilitation for respiratory diseases 34 ) . In contrast, reports of aerobic exercise, stretching, and comprehensive physical therapy have not shown substantial improvement. We speculate that confounding factors, such as study design, intervention method, and duration and frequency of interventions, may contribute to this difference. For example, these reports are case-series studies, and the lack of a control group makes testing for differences difficult; thus, determining a generalized effect is not possible. Additionally, improvements due to resistance training, aerobic exercise, and stretching, regardless of whether the patients were in a telemedicine environment or not, lacked evidence 30 , 31 ) . Furthermore, the intervention period reported by Braga et al. 18 , 19 ) was six months, but maintaining physical function and ADL for six months in this rapidly progressing disease was difficult. In terms of the content of telerehabilitation, Braga et al. 18 , 19 ) and De Marchi et al. 21 ) reported that the frequency of intervention was approximately once a week, and Burke et al. 20 ) provided on-demand video instruction without real-time instruction. Telemedicine increases the workload of biomonitoring data analysis and data protection and places a heavy administrative burden on healthcare providers 18 , 19 ) . Based on these results, determining the effectiveness of aerobic exercise, stretching, and comprehensive physical therapy is difficult.

In a report by Braga et al. 18 , 19 ) on adverse events, the maximum heart rate temporarily exceeded the expected value, but real-time monitoring by a tele-monitoring system allowed rapid correction, preventing adverse events through telerehabilitation. However, three reports did not describe adverse events, and the safety of telerehabilitation was unknown.

Patient satisfaction was generally high; Kiefer 22 ) reported a mean score of 4.0 on a survey using the Telemedicine Satisfaction Questionnaire. The mean score of satisfaction with Telemedicine Satisfaction Questionnaire was 3.5–4.4 in patients with neurodegenerative diseases 35 , 36 ) , which was similar to that reported by Kiefer 22 ) The items with lower satisfaction were operability of the equipment, cost, and quality of care equivalent to face-to-face care. The following issues in telerehabilitation have been highlighted: unstable internet connection in some areas, complicated operation of equipment for older individuals, cost of purchasing equipment, and limitations of evaluation based on communication through a screen 37 , 38 ) . The items with low satisfaction in this study were similar to these concerns, suggesting that they are not disease-specific issues, but rather general challenges in telerehabilitation that also apply to ALS.

As expected, few reports focused on the telerehabilitation of patients with ALS, and the selected articles were case-control or case-series studies of a small number of patients; thus, the findings were limited. However, telerehabilitation for patients with ALS improved adherence. Particularly, respiratory rehabilitation significantly improved physical function and ADL. Patient satisfaction was generally high. The results suggest that telerehabilitation can be used to educate and manage patients to individually master appropriate exercise intensity and exercise methods at home.

Regarding the limitations and future perspectives of this study, we only included articles written in Japanese and English; therefore, the influence of language bias cannot be ruled out. Second, the number of studies was particularly small, and reports of high-quality studies such as randomized controlled trials, interventions for severe cases, and studies using the latest technologies such as artificial intelligence were not identified. However, randomized controlled trials are ongoing 39 , 40 ) , so more high-quality studies are expected to be conducted in the future to establish appropriate telerehabilitation according to symptoms and severity. Additionally, although we confirmed an improvement in adherence, most of the results were based on self-reports by patients or family members, which may not accurately reflect true adherence because of potential omissions or incorrect performance. Moreover, burden on patients and providers associated with telerehabilitation must be considered. Patients may experience operational complexity and financial burdens, while healthcare providers may face an increased administrative workload. To solve these problems, simple technology, artificial intelligence, and support and education systems are required. Finally, when considering the implementation of telerehabilitation, institutional differences across countries should be taken into account. For example, in Japan, telerehabilitation is currently not covered by public medical insurance, and a well-developed long-term care insurance system exists. These factors may affect the demand and feasibility of telerehabilitation, and similar contextual considerations may apply in other countries.

Funding

The authors received no funding, grants, or equipment for this research from any source or financial benefit.

Conflict of interest

The authors declare no conflicts of interest.

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