Effect of Dual-Task Motor-Cognitive Training in Preventing Falls in Vulnerable Elderly Cerebrovascular Patients: A Pilot Study

Falling is a frequent and major clinical problem among older adults, as well as in patients with chronic cerebrovascular diseases (CVD). At present, sequential (mixed) and simultaneously (dual-task) motor-cognitive trainings are the best approaches to affording patients more autonomy in their everyday motor independence while reducing fall risks and consequences. The objective of this study was to evaluate the efficacy of an advanced and innovative dual-task motor-cognitive rehabilitation program on fall risks in vulnerable older persons with chronic CVD. To this purpose, 26 consecutive older fallers with chronic CVD were recruited, and completed a mixed motor-cognitive or a dual-task motor-cognitive training program. Each patient also underwent two test evaluations to assess balance, gait, fear of falling, and walking performance at pre-and post-intervention. We found that our experimental motor-cognitive dual-task rehabilitation program could be an effective method to improve walking balance, gait, walking speed, and fear of falling, while reducing the risk of falls in older people with chronic CVD. Furthermore, results show that the simultaneous motor-cognitive training is more effective than the sequential motor-cognitive training. Therefore, our study brings innovative data, which can contribute positively to the management of this population.


Introduction
Falling is a frequent and major clinical problem with potentially severe consequences in the elderly [1].It is estimated that 20 to 30% of older adults fall each year [2].Though not all falls are serious enough to require medical attention, it is known that all falls are predictors of future falls; they can lead to fear of falling, and can restrict a person's activities of daily living [3,4].
In geriatric medicine, falls are considered a syndrome with multiple causes and contributors [5].Chronic cerebrovascular diseases (CVD) are common diseases that endanger the health of older adults who are at high risk of imbalance or falls [6].The overlap between CVD and falls is well established [4].Both have a negative prognosis in elderly individuals in terms of mortality and morbidity [7].Falls in patients with CVD are usually attributed to a combination of factors that may or may not be related to CVD, and CVD is just one of the many significant comorbidities that affect older adults [8].Most older patients with CVD fall inside their homes; in fact, it has been reported that walking and transfers are the most frequent activities at the time of a fall [9].A significant number of these falls Brain Sci.2022, 12, 168 2 of 14 result in soft tissue injuries, fractures, and the need for medical interventions.Falls can also lead to limitations in the performance of daily living activities, increased dependence, development of fear of falling, and low fall self-efficacy [10][11][12][13].Thus, both serious and non-serious falls are still among the most common complications in CVD patients, and their increasing incidence poses a challenge for rehabilitation [4].
Few studies have examined fall prevention in CVD patients.However, interventions recommended for the general older population who have experienced falls have been reported [4].Evidence highlights the efficacy of different types of interventions to prevent falls in the elderly [14,15].It has been emphasized that programs to prevent falling should include multifactorial and exercise interventions, and should aim at improving cognitive functions [15,16].
The relationship between motor and cognitive skills and falls becomes evident if we consider that, in everyday life, walking is a very attention-demanding task that requires a high level of mobility skill and cognitive flexibility to plan and execute movements [17].In this perspective, in dual-task situations, i.e., when an individual is required to walk and carry out another task simultaneously, such as during the activities of daily living, the increased cognitive demand may lead to worse performance on both tasks, and a greater risk of falling [18].This problem is most prominent in older adults and in CVD patients because of their impaired motor and cognitive abilities [19][20][21].
Evidence suggests that an intervention which integrates cognitive training with standard motor training is the best approach to ensure that patients are more autonomous in their everyday motor activities, thus reducing the risk of falling and its consequences [6,16,22,23].
Furthermore, in a growing body of research, it has been shown that motor-cognitive dual-task training (i.e., cognitive rehabilitation training at the same time as exercise rehabilitation therapy) can enhance the effectiveness of patients' physical motor function rehabilitation [6,24].Additionally, there is increasing interest in the use of rehabilitation technology, such as virtual reality and robotics, to address balance and gait, to improve mobility, and prevent the risk of falling [23,24].
Thus, the aim of this study was to evaluate the efficacy of an advanced and innovative dual-task motor-cognitive rehabilitation program on the risk of falling in older persons with chronic CVD.This intervention model might have several advantages compared to standard rehabilitation protocols: the experience is engaging and captivating; the use of technologies allows greater flexibility in developing and proposing exercises adapted to the clinical aims, and with increasing levels of difficulty; the implementation of the exercises can be adapted to different types of cognitive profiles, so patients can experience a non-monotonous and interesting rehabilitation experience.
We hypothesized that when compared to separate traditional treatments (i.e., mixed motor and cognitive rehabilitation programs), our dual-task rehabilitation program involving cognitive and motor tasks simultaneously leads to a reduced risk of falling due to the improvement of balance and gait.

Participants and Study Design
Twenty-six consecutive older fallers with chronic CDV (i.e., ischemic and/or hemorrhagic stroke) presenting at the IRCCS Santa Lucia Foundation were randomly assigned to the mixed motor and cognitive (MixT), group (n = 13), or dual-task motor-cognitive training (DTT) group (n = 13).
All patients underwent a clinical screening that included the collection of medical history, history of previous falls, and the administration of the Tinetti Performance Oriented Mobility Assessment (POMA) [25,26].
Eligible participants were older adults (aged ≥ 65 years) with CVD and with a formal education of at least 5 years who met the inclusion eligibility criteria for risk of fall according to previous studies [16] (total POMA score ≤ 20 and/or at least one fall in the previous year).The presence of major cognitive disturbances; a history of behavioral, psychiatric, and/or systemic disturbances; and/or receiving any rehabilitative treatment represented exclusion criteria.

Mixed Motor and Cognitive Training (MixT)
Those participants randomized into MixT underwent individual combined/mixed motor and cognitive treatments, resulting in 30 min of motor training and 30 min of cognitive training per session.The intervention program was administered through five weeks with three weekly sessions, totaling fifteen sessions.The MixT program is summarized in Table 1.
Motor training consisted of a set of warm-up procedures (i.e., stretching and squatting), followed by exercises dedicated for the halftime of each session to balance and halftime to gait.Balance training consisted of exercises lifting up heels or tiptoes, lateral/forward shifting, and holding and flexion/extension exercises.Gait exercises involved forward and backward walking over the ground with several variants and without use of assistive devices.To prevent errors, verbal instructions were provided by the therapist to assist patients in exercise executing (e.g., "correct head position", "correct feet position", "correct balance").All exercises were augmented in difficulty by increasing speed, repetition, and changing holding position (see Table A1 for a description of each motor exercise) Cognitive training consisted of a set of exercises mainly focused on executive functions and attention (2/3 of the time of each training session).These were provided by trained cognitive therapists in an individual setting administered through a computerized touch-screen platform (either in a table or in an all-in-one desktop computer) [16].Each exercise provided three increasing levels of difficulty (i.e., easy, intermediate, hard), adjusted by the therapists according to the subject's capability, and starting with the easiest one and increasing after two sessions at the highest level.In particular, executive function exercises consisted of abstraction tasks, planning, and working memory (e.g., ordering at a restaurant following some rules; solving tasks on similarities, differences and analogies; sorting pictures guessing a covered criterion), whereas attention exercises consisted of selective and sustained attention tasks (e.g., paying attention to a target item among distractors).Exercises of other main cognitive functions (i.e., declarative memory, spatial orientation, constructional praxis, language, and abstract reasoning) were executed during the remaining 1/3 of the time of each training session [16].(See Table A2 for a description of each cognitive exercise).
Intensity of each MixT session was patient-specific, with rest breaks provided upon therapist discretion and patients' tolerance to activity.

Motor-Cognitive Dual-Task Training (DTT)
Those participants randomized into DTT underwent an individual experimental dualtask rehabilitation program.This consists of simultaneous administration of motor and cognitive tasks, stimulating patients to enhance both abilities, in a dedicated room, resulting in 40-min of training per session.All the exercises proposed were developed by the research team on the basis of specific technological properties of the applied aid.
The intervention program was administered through five weeks with three weekly sessions, totaling fifteen sessions.The DTT program is summarized in Table 1.
The first part of the DTT protocol (1/3 of the time of each training session) concerned the use of the sensory carpet (2 m), which presents diverse surfaces (medium density smooth, sandy, and cobbled), and a video projector.The exercises have been developed to stimulate balance and gait motor skills, and cognitive abilities, such as attention (alert, target visuospatial search), visual-spatial associative memory, language (reading and calculating), and executive functions (verbal judgments and cognitive estimates).
Examples of exercises are: following the traffic lights, the environmental scenarios inclusive of the congruent and incongruent sounds, the association of sounds and images to remember, walking while looking for numbers and making calculations.The second part of the protocol (2/3 of the time of each training session) concerned the use of a led floor (4.5 m × 1.5 m) and five video projectors (see Figure 1).We used an adapted version of the Walking Stroop carpet (WSC) used by Perrochon et al. [27] to detect cognitive impairment.The surface on which the patient walked was stable, and proposed different paths (follow the line, avoid the holes, center the box).The cognitive stimuli changed and required different cognitive functions: attention (visual-spatial research and attentional shifting), executive functions (interference inhibition, go/no go, updating), long-and short-term visuospatial memory, and language (denomination, calculation) (see Table A3 for a description of each cognitive exercise).
the use of a led wall (4.5 m × 1.5 m) and five video projectors (see Figure 1).The surface on which the patient walked was stable, and proposed different paths (follow the line, avoid the holes, center the box).The cognitive stimuli changed and required different cognitive functions: attention (visual-spatial research and attentional shifting), executive functions (interference inhibition, go/no go, updating), long-and short-term visuospatial memory, and language (denomination, calculation) (see Table A3 for a description of each cognitive exercise).
All the abilities are trained according to increasing levels of difficulty (except for the "Walking Stroop" and "Walking Trail Making Test" exercises, which do not present increasing levels of difficulty, but two phases that constitute the entire exercise to be administered consecutively).This allowed the personalization of the program according to patients' needs.
To prevent errors, verbal instructions were provided by the therapist to assist patients in exercise executing (e.g., "correct head position", "correct feet position", "correct balance").
Intensity of each DTT session was patient-specific, with rest breaks provided upon therapist discretion and patients' tolerance to activity.All the abilities are trained according to increasing levels of difficulty (except for the "Walking Stroop" and "Walking Trail Making Test" exercises, which do not present increasing levels of difficulty, but two phases that constitute the entire exercise to be administered consecutively).This allowed the personalization of the program according to patients' needs.
To prevent errors, verbal instructions were provided by the therapist to assist patients in exercise executing (e.g., "correct head position", "correct feet position", "correct balance").
Intensity of each DTT session was patient-specific, with rest breaks provided upon therapist discretion and patients' tolerance to activity.

Outcomes
To assess the impact of different training on risk of falls, each patient underwent two evaluations, one within 1 week before the start of the study (MixT or DTT), and one within 1 week after the intervention (5 weeks later).Assessments were performed through standardized scales, and included: (1) evaluation of motor performance aimed at balance and gait with Tinetti Performance Oriented Mobility Assessment (POMA) for balance (POMA-B) and gait (POMA-G) [25,26]; (2) evaluation of fear of falling with the Falls Efficacy Scale-International (FES-I) [10,28]; (3) evaluation of physical performance Brain Sci.2022, 12, 168 5 of 14 with the six-minute walking test (6-MWT) [29,30], and gait speed (calculated as 6-MWT distance in meters divided by 360 s).

Tailoring
The intervention of both MixT and DTT groups was adjusted according to the subject's capability.
Before training, therapists make a simple and rapid assessment of patients to select the personalized intervention intensity suitable for patients.Programs can also be adjusted according to patients' own preferences.The intensity of each session was patient-specific, with rest breaks provided upon therapist discretion and patients' tolerance to activity.Each exercise provided increasing levels of difficulty adjusted by the therapists, consistent with the subject's capability.Continuous variables are reported as mean ± standard deviation.Categorical variables are reported as frequency and percentage.Differences in the demographic data of the groups were tested using either the Mann-Whitney U test or χ 2 test according to the level of measurement.
The within-group effects (i.e., the difference in the outcomes observed between T0 and T1) were examined by employing the Wilcoxon signed-ranks test.We adopted this nonparametric test because the sample size was small.We also report the Z-score to represent the within-group effect size.
Change values for the outcome measures were calculated by subtracting the baseline data from the post-intervention data.To analyze between-group improvement, the change values were analyzed using the Mann-Whitney U test.
For the outcome, after the Bonferroni correction, the statistically significant threshold was set at p < 0.008.

Discussion
In this study, we aimed to evaluate the efficacy of our experimental, motor-cognitive, dual-task rehabilitation program (DTT), developed within a dual-task room, on the risk of falling in vulnerable older patients with chronic CVD, compared to a conventional mixed motor-cognitive training (MixT).
It is known that both MixT (i.e., motor and cognitive trainings are conducted separately) and DTT (i.e., motor and cognitive trainings are conducted simultaneously) are effective in improving physical performance (e.g., balance, gait, walking speed) and fear of falling in older adults and stroke patients [6,16,[31][32][33][34].However, clinical evidence which shows that DTT is more effective than its sequential counterpart is lacking.
Furthermore, to the best of our knowledge, this is the first pilot study that compares the effects of a simultaneous vs. a sequential motor-cognitive training program in reducing the risk of falling in older individuals with chronic CVD.Therefore, our study provides innovative data that can contribute positively to the management of this population.
According to our findings, the experimental motor-cognitive dual-task rehabilitation program is an effective method for improving walking balance, gait, and walking speed, as well as reducing the fear of falling.It also leads to a reduced risk of falls in older people with chronic CVD.Furthermore, DTT is a more effective approach than MixT.
Results show that both groups (i.e., the experimental DTT and the conventional MixT) improved, but only the dual-task intervention was effective in mobility (POMA-total) in both balance (POMA-B) and gait (POMA-G) components, and in fear of falling (FES-I).
However, the superiority of this treatment over the conventional one was specifically found only for mobility (POMA-tot) and its gait component (POMA-G).
This slight superiority obtained in the DTT group in the studied variables seems to be related to the specificity of this training, because it incorporates dual-task cognitive-motor aspects that are so important for this population.
First, in the case of the POMA test, similar findings on the balance component (POMA-B) only suggest that our DTT intervention is more effective in enhancing dynamic/walking balance than static/standing balance.In this regard, an improvement in the general balance condition may have been promoted by weight transfer and dynamic postural adaptation.Although we can only speculate about these findings, we propose that the POMA-B is Brain Sci.2022, 12, 168 9 of 14 more sensitive for assessing the static balance component.In fact, in the POMA-B, balance is assessed while the person being evaluated is sitting, arising, standing (immediate and prolonged), and turning.On the other hand, the POMA-G component test, which includes initiation, step length and height, step symmetry, step continuity, walking path, trunk sway, and walking stance (width), could be an indirect measure of dynamic/walking balance.
Consistent with this speculation, it was reported that an unstable support surface, such as that used in our DTT protocol, stimulates tactile sensation, vestibular sensations, proprioceptive sensations, etc., to induce posture and balance reactions, and, thus, promote dynamic stability [35].
Furthermore, a recent RCT-based meta-analysis [6] reported that the improvement effect of cognitive-motor dual-task training on the walking balance of chronic stroke patients was significantly better than that in the control group.
Second, although the DTT intervention did not statistically improve walking performance (6-MWT and/or gait speed), it is noteworthy that, in the DTT group, walking endurance (6-MWT distance) and gait speed were improved by 34 m and 0.10 m/s, respectively.Similar to our findings, Barboza et al., [36] and Liu et al. [32] found no significant differences between the group that received the motor plus cognitive training [36] or the cognitive-motor dual-task [32] than the group that received only motor training and/or the motor-motor dual-task.Nevertheless, our findings on walking performance are interesting, considering that it has been reported that an improvement of 0.10 m/s for gait speed, and an improvement of 20 m for 6MWD, are considered clinically meaningful changes [37].
Third, regarding the FES-I results, only the DTT intervention was effective in reducing fear of falling in older people with chronic CVD.It is also relevant that the patients who underwent the DTT obtained an FES-I score of 28, which is considered the cut-off score for classifying fallers and non-fallers [10].On the other hand, these findings fit with our other study results, and are in line with a parallel outcome in the literature.In a recent study, Sampaz Mujdeci et al. [3] showed that fear of falling negatively affects balance performance; Lopes et al. [38] found a correlation between fear of falling and dynamic balance and mobility; and another study [39] found a very high relationship among fear of falling, functional mobility, and balance.Likewise, here, we found that changes in fear of falling parallel changes in balance and mobility performance.
This study also suffers from a series of limitations.First, the sample size is small.This limits confidence in the effects that were observed, and makes it difficult to generalize the results.A larger, randomized, controlled clinical trial is needed to validate the reported benefits of the dual-task training protocols reported in the current study.Second, because there was no follow-up test, it was impossible to demonstrate whether improvements could be maintained.Third, the lack of a cognitive assessment did not allow us to evaluate the effect of treatment on cognitive performance.Indeed, future research should consider this issue.

Conclusions
This study presents an alternative intervention for older people with CVD.The preliminary results suggest that our DTT can have (has) an adequate influence on the improvement of walking balance, gait, walking endurance and speed, and fear of falling.Future studies should replicate this pilot study by employing a larger sample, so that its effects can be more confidently evaluated.Sensory carpets (medium density smooth, sandy, and cobbled) Subtraction: the user is asked to walk forward on a carpet by subtracting from 50, one (i.e., 50-1; easy), two (i.e., 50-2; medium), or three (i.e., 50-3 difficult) numbers.
Sounds: the user is asked to walk forward on a carpet by listening a sound (e.g., sound of bell, phone, intercom, train, rain, etc.; easy), by listening a sound and naming it (medium), or by listening a sound and making a judgment (i.e., natural/artificial, coherent/incoherent) on it (difficult).
Letters and words: the user is asked to walk forward on a carpet by saying the letters of the alphabet out loud (a letter at every step; easy), by saying words that begin with a certain letter (medium) out loud, or by saying words that belong to a certain category out loud (e.g., animals; difficult).Go/No go: the user asked to walk forward on a carpet respecting congruent (i.e., walk at a green light, and stop at a red light; easy), or incongruent (i.e., stop at a green light, and walk at a red light; easy) signals projected on a screen.
Walking Stroop: the user is asked to walk forward a walkable led floor with black words naming colors (e.g., red, yellow, green, blue), following words naming a color (e.g., yellow), and saying the color out loud (e.g., yellow) (easy); or to walk forward on a walkable led floor with colored words, naming correspondent (e.g., word "green" colored in green) and non-correspondent colors (e.g., word "red" colored in green), following words' colors in a certain color (e.g., all words colored in green), and saying the followed color out loud (e.g., green) (medium); or to walk forward on a walkable led floor with colored words, naming correspondent (e.g., word "yellow" colored in yellow) and non-correspondent colors (e.g., word "yellow" colored in red), following words naming a certain color (e.g., all words "yellow") and saying the followed color out loud (e.g., "yellow") (difficult).(Figure A1) Walking Trail Making Test: the user is asked to walk forward on a walkable led floor with numbers or numbers + letters following in ascending order (from 1 to 20 and/or from a to z) numbers (easy), or numbers + letters (difficult).
Avoid the holes: the user is asked to walk forward on a walkable led floor that simulates a street, avoiding holes that appear on one side (easy) or on both sides (medium) of the street, and by following the directions on signs projected on a screen (e.g., stop, raise your arms).
Shopping list: the user is asked to walk forward on a walkable led floor that simulates a street by looking at (projected on a screen) or listening to some shopping list items (e.g., milk, eggs, soap).She/he is asked to cross the street by remembering the shopping list.

Figure 1 .
Figure 1.Dual-task room: five screens; one walkable led floor 4.5 m × 1.5 m; one audio/video controller console.Figure 1. Dual-task room: five screens; one walkable led floor 4.5 m × 1.5 m; one audio/video controller console.

Figure 1 .
Figure 1.Dual-task room: five screens; one walkable led floor 4.5 m × 1.5 m; one audio/video controller console.Figure 1. Dual-task room: five screens; one walkable led floor 4.5 m × 1.5 m; one audio/video controller console.

Figure A1 .
Figure A1.Example of a walkable led floor representation during an easy, medium, or difficult DTT Walking Stroop task.See Table A3 for more details.A figure was reproduced, with the permission of the authors, from Figure 1B-D in Clinical interventions in Aging, Walking Stroop carpet: an innovative dual-task concept for detecting cognitive impairment, Clinical Interventions in Aging 2013, 8, 317-328 by Perrochon et al. [27].

Table 1 .
Summarized description of MixT and DTT interventions.
Abbreviations: MixT: combined motor and cognitive training; DTT: motor-cognitive dual-task training.See text and Appendix A for more details.

Table 2 .
Patients' demographic and clinical results at baseline.
Abbreviations: MixT: combined motor and cognitive training; DTT: motor-cognitive dual-task training; p value, between-group difference; POMA tot: Tinetti Performance Oriented Mobility Assessment total score; POMA-B: POMA balance score; POMA-G: POMA gait score; FES-I: Falls Efficacy Scale-International score; 6-MWT: 6-min walk test; m = meters; s = seconds.a Values are mean ± SD, b Values are number.See text for more details.

Table 3 .
Outcome performance after different training protocols.

Table 3 .
Outcome performance after different training protocols.
Abbreviations: MixT: combined motor and cognitive training; DTT: motor-cognitive dual-task training; p value, between-group difference; POMA-tot: Tinetti Performance Oriented Mobility Assessment total score; POMA-B: POMA balance score; POMA-G: POMA gait score; FES-I: Falls Efficacy Scale-International score; 6-MWT: 6-min walk test; m = meters; s = seconds.a Values are mean ± SD. b Change values were calculated by subtracting the pre-training data from the post-training data.See text for more details.

Table A3 .
Exercises of motor-cognitive dual-task training in the DTT protocol.