People with Dementia Can Learn Compensatory Movement Maneuvers for the Sit-to-Stand Task: A Randomized Controlled Trial

Abstract

Background:

A complex motor skill highly relevant to mobility in everyday life (e.g., sit-to-stand [STS] transfer) has not yet been addressed in studies on motor learning in people with dementia (PwD).

Objective:

To determine whether a dementia-specific motor learning exercise program enables PwD to learn compensatory STS maneuvers commonly taught in geriatric rehabilitation therapy to enhance patients’ STS ability.

Methods:

Ninety-seven patients with mild-to-moderate dementia (Mini-Mental State Examination: 21.9±2.9 points) participated in a double-blinded, randomized, placebo-controlled trial with 10-week intervention and 3-month follow-up period. The intervention group (IG, n = 51) underwent a motor learning exercise program on compensatory STS maneuvers specifically designed for PwD. The control group (CG, n = 46) performed a low-intensity motor placebo activity. Primary outcomes were scores of the Assessment of Compensatory Sit-to-stand Maneuvers in People with Dementia (ACSID), which covers the number of recalled and initiated, and of effectively performed compensatory STS maneuvers. Secondary outcomes included temporal and kinematic STS characteristics measured by a body-fixed motion sensor (BFS, DynaPort^® Hybrid).

Results:

The IG significantly improved in all ACSID scores compared to the CG (p < 0.001). Secondary analysis confirmed learning effects for all BFS-based outcomes (p < 0.001–0.006). Learning gains were sustained during follow-up for most outcomes.

Conclusion:

People with mild-to-moderate dementia can learn and retain compensatory STS maneuvers in response to a dementia-specific motor learning exercise program. This is the first study that demonstrated preserved motor learning abilities in PwD by using a motor skill highly relevant to everyday life.

Keywords

Dementia learning motor skills movement randomized controlled trial rehabilitation

INTRODUCTION

Motor skills, defined as goal-directed activities that involve voluntary body, head, and/or limb movements [1], are learned throughout the lifespan. People need to acquire new motor skills to cope with the changing environment, to adapt or modify motor skills to age-related changes in cognitive and motor abilities, and to relearn previously acquired motor skills that have been compromised due to diseases or injuries [2, 3].

Although deficits in cognitive functioning (e.g., memory, attention, executive functions, information processing speed, perception) may seriously hamper motor learning capabilities in older adults [4 –6], a number of studies reported preserved motor learning in people with dementia (PwD) [6 –11]. Previous findings are, however, based on experimental, low-complexity, fine (e.g., rotary pursuit task, maze test, serial reaction time task) [6 , 9–11] or gross motor tasks (tossing a beanbag on a target) [12], or a complex gross motor task with limited relevance to everyday functioning (waltz dancing) [8]. A complex motor skill highly relevant to functional mobility in everyday life has so far not been addressed by studies on motor learning in PwD. In addition, previous studies most frequently focused solely on the initial acquisition of a motor task after several learning trials within few practice sessions and/or did not include follow-up assessments after long-term periods without training to evaluate the long-term retention and sustainability of learning effects [6 , 13–16].

A key motor skill for everyday life is rising from a seated to a standing position, which represents one of the most complex functional tasks in the activities of daily living. Involving the motion of all body segments, the sit-to-stand (STS) transfer requires adequate muscle strength, joint mobility, motor planning and control, and balance ability [17 –19]. However, as a consequence of the aging process, these subject-related determinants for successfully completing the STS movement decrease with age [20 –22], and many older adults have difficulties in performing a STS transfer [23, 24]. In nursing home residents, the STS transfer has even been identified as the leading cause (‘hotspot’) of falls [25]. In addition to the age-related decline in motor function, PwD have shown disease-related disorders in the motor action organization of the STS transfer [26], indicating that cognitive impairment may also have a detrimental effect on the STS ability. Spatiotemporal features in the STS motion of PwD have been reported to differ significantly from those of healthy elderly, in terms of a reduced forward trunk flexion coupled with an earlier initiation of the trunk and lower limb extension [26]. The use of such a dominant vertical STS movement strategy is associated with a higher maximum knee torque and requires greater muscular strength in lower extremities to reach the standing posture, thus decreasing the overall STS movement quality and efficiency [18, 26]. Such motor behavior may be particularly due to the decline in attention control of executive functions [26], which is among the earliest symptoms of dementia along with amnesia [27]. Executive functions are defined as higher-order cognitive functions that are necessary to plan, initiate, control, and execute a sequence of goal-oriented complex actions [28]. However, PwD may lose their capacity of integrating such high-level, cognitive aspects of motor processes (i.e., preparing, controlling and executing efficient body motions) into motor action organization [26 , 29], which might be linked to the extraordinary high fall incidence reported for PwD [30].

During STS (re-)training in geriatric rehabilitation therapy, the STS transfer is broken down into individual motion components (e.g., feet displacement, trunk flexion, standing up) to reduce the complexity, to decelerate the total movement speed, and to facilitate the motor learning process during rehabilitation. For these STS components, specific movement maneuvers are then commonly taught to compensate for deficits in subject-related STS determinants (e.g., muscle weakness, balance disturbances, impaired motor planning/control) and thus to enhance a patient’s STS ability. These ‘compensatory’ STS maneuvers include, in serial order, an anterior buttocks displacement to the front edge of the chair seat [31, 32], a posterior feet displacement behind the knees [33, 34], straightening and stabilizing the upper body to an extended, active sitting posture [35], and excessive trunk flexion before rising to an upright standing position [32, 36]. To our knowledge, no study has so far investigated whether PwD can learn such compensatory STS maneuvers.

Learning these movement maneuvers initially requires a patient’s ability to memorize the motor actions in order to be able to adequately recollect and initiate them later on (‘what to do’). In a second step, a patient’s attention has to be focused on the movement control and execution of the initiated maneuvers in order to effectively perform them as intended (‘how to do’). Due to the decline in memory, attention, and executive functions, PwD may, however, have difficulties in both domains. STS (re-)training programs on compensatory STS maneuvers should therefore provide practice conditions and apply teaching methods specifically adapted to the abilities of PwD to facilitate motor learning of these maneuvers.

Several theories of motor learning (e.g., schema theory [37], theories of contextual interference [38], differential learning [39]) propose that practicing a motor skill under variable conditions leads to superior learning effects. Early research on learning of experimental motor skills has, however, demonstrated that PwD learn best under constant practice conditions, in which the same tasks or movements are practiced repeatedly without variations [12 –14]. For (re-)learning instrumental activities of daily living (IADLs, e.g., use of a calendar, microwave, coffee maker, etc.) in PwD, it has been reported that errorless learning methods, which aim at reducing the likelihood of making errors throughout the learning process [40], were effective (for review, see [41]). The error reduction may be achieved by a variety of teaching methods and task adaptions such as parts-to-whole practice, modeling task steps, verbal instructions, or cueing [41]. The practice conditions and teaching methods known to facilitate (re-)learning of experimental, low-complexity motor skills or IADLs in PwD have not yet been used in a previous study in order to teach PwD movement maneuvers for a complex gross motor task by a dementia-specific exercise program.

In summary, the primary aim of this study was to test the hypothesis that people with mild-to-moderate dementia can learn compensatory STS maneuvers in response to a dementia-specific motor learning exercise program. A secondary aim was to evaluate the sustainability of potential learning effects.

MATERIAL AND METHODS

Study design

The study was designed as a double-blinded, randomized, placebo-controlled 10-week intervention trial with a 3-month follow-up period. Neither the investigators nor the participants were aware of group identity. The ethics committee of the Medical Department of the Heidelberg University approved the study in accordance with the Declaration of Helsinki. Written informed consent was obtained from all participants (or legal representatives) prior to study inclusion. The trail was registered at www.isrctn.com (ISRCTN37232817).

Study population

Participants were consecutively recruited from rehabilitation wards of a German geriatric hospital, from nursing homes, and from a community-dwelling population. Eligible participants were screened for cognitive impairment using the Mini-Mental State Examination (MMSE) [42]. In those with MMSE scores from 17 to 26, a comprehensive neuropsychological testing was performed by using the Consortium to Establish a Registry for Alzheimer’s Disease (CERAD) test battery [43] with a modified Trail Making Test (ZVT-G) [44] and a digit-span test (ZN-G) [44]. Only individuals meeting predefined criteria for probable dementia in the neuropsychological testing (test scores below the 10th percentile [z-score –1.28] of the normative sample on at least one memory test and one other neuropsychological test [45, 46]) were included in the study. Further inclusion criteria were: ≥65 y; no severe neurologic, cardiovascular, metabolic, or psychiatric disorders; residence within 15 kilometers of the study center; ability to walk at least 10 meters without a walking aid; and written informed consent. Patients meeting the inclusion criteria were randomly assigned to the intervention group (IG) or the control group (CG) using the urn design for clinical trials (numbered containers), with stratification according to sex and location of recruitment (rehabilitation wards versus others) [47]. A person unrelated to the study performed the randomization procedure.

Intervention

Participants assigned to the IG took part in a dementia-specific motor-cognitive training program for 10 weeks (1.5 h, twice a week) conducted in groups of maximum 7 participants and supervised by 2 qualified trainers experienced in training PwD. Within each group session, participants performed a motor learning exercise program on the compensatory STS maneuvers for 15 min. Other training components were a motor-cognitive dual-task training (‘walking while counting’) and a computerized, game-based motor-cognitive training on an interactive balance platform (‘exergaming’).

Based on the findings of previous studies on learning of motor skills or IADLs in PwD [7, 41] and recommendations given for promoting physical exercise in PwD [48, 49], specific teaching methods and practice conditions were used to facilitate learning of the compensatory STS maneuvers: parts-to-whole practice, verbal instructions and cueing, modeling task steps (mirror technique), haptic assistance, constant practice with high repetitions, verbal praise, and immediate error correction.

The STS movement was initially broken down into five constituent components for parts-to-whole practice [50]: (1) anterior buttocks displacement; (2) posterior feet displacement; (3) trunk straightening; (4) excessive trunk flexion; and (5) standing up. Referring to a method also used in mental practice [51], each of these components was symbolically marked by a direct and concise verbal cue that clearly described the movement maneuver to be performed (e.g., ‘slide forward to the front edge of the chair seat’). During repeated step-by-step demonstration, the trainer constantly modeled each movement maneuver in combination with its specific cue in order to prompt participants for movement, to direct their attention to the specific components of the STS transfer, to enhance the movement preparation and initiation, and, overall, to facilitate the storage and recall of the trained movement maneuvers [52]. Participants were encouraged to immediately join the demonstrations, follow the cues given, and mirror trainer’s movements. If necessary, haptic assistance was provided by another trainer to ensure correct and effective movement execution of the participants. The STS movement was sequentially demonstrated and taught by using a forward chaining method. That is, starting with training on the first component, each subsequent component was added in the teaching process after the participants had mastered the previous one(s). This forward progression continued until all components were included in the ‘chain’ and participants were able to mirror and perform the entire ‘compensatory STS movement strategy’ without errors. For each learning step, extensive practice under constant conditions (i.e., same task without variation, trainer demonstration with cues, haptic assistance) with a large number of repetitions was provided. Any progress in learning was consequently praised by trainers. As training progressed, external assistance by trainers was gradually faded (‘vanishing cues’) [53], in such a way that eventually participants were able to perform the movement strategy independently. At first, haptic assistance was no longer provided, and in subsequent steps, the verbal cues given by the trainer during the demonstration became gradually shorter (e. g., ‘slide forward to the front edge of the chair seat” to ‘slide forward’). As a last step, the demonstration by trainer was withheld and participants were asked to demonstrate the movement strategy in front of the training group and to simultaneously prompt the other participants using the verbal cues learned [54]. To promote participants’ own error detection and correction abilities, the other participants were encouraged to check the demonstration and instructions of their fellow participant and to intervene and provide help if the demonstrating participant was unable to recall or missed any of the components of the compensatory STS movement strategy. When errors remained undetected or wrong, corrections were given by participants, the procedure was immediately interrupted, and the demonstrating participant received assistance from trainers.

The CG met two times a week for one hour of motor placebo group training, including unspecific, low-intensity strength and flexibility exercises for the upper body while seated supervised by the same two trainers of the IG.

In both training groups, much attention was paid to emotional aspects such as reassurance, respect, and empathy toward the participants as described in dementia-care guidelines [55]. A free transportation service to and from study sessions was provided for all participants as part of the dementia-specific, patient-centered approach.

Study participants were blinded since they had not been informed about group allocation and the potential different effectiveness of the two training regimens, which prevented expectations of the training effects.

Training adherence was documented at each training session and calculated as the ratio of the number of training sessions attended to the total number of sessions prescribed (i.e., 20 sessions), multiplied by 100.

Descriptive measurements

Demographic and clinical characteristics assessed at baseline including age, gender, education, comorbidity (number of diagnoses), medication (number), falls in the previous year, and social status (comm-unity-dwelling versus institutionalized) were documented from patient charts or by standardized patient interviews. A trained interviewer assessed psychological status for depression (Geriatric Depression Scale, 15 item version [56]), health-related quality of life (12-item Short Form Health Survey [57]), and fear of falling (7-item Short Falls Efficacy Scale-International [58]). Functional status was measured by the Performance Oriented Mobility Assessment (POMA) [59] and the Timed Up and Go (TUG) [60].

STS measurements

Standardized STS measurements were performed before (T1) and at the end of the 10-week training intervention (T2), and after the 3-month follow-up period without training (T3). All measurements were administered by a blinded person who had been adequately trained in test procedure and in measuring PwD [61].

Assessment of Compensatory Sit-to-stand Maneuvers in People with Dementia

Participants’ STS transfers were evaluated by the observation-based Assessment of Compensatory Sit-to-stand Maneuvers in People with Dementia (ACSID) [62]. The ACSID had been specifically developed and validated for use in PwD to document motor and cognitive aspects in the movement process of the compensatory STS maneuvers commonly taught in geriatric rehabilitation therapy. The items of the ACSID assess each of the five maneuvers of the compensatory STS movement strategy by a cognitive dimension, which covers the ability to explicitly and consciously recall and initiate the maneuvers (‘recall and initiation’, RI), and a motor dimension (‘effective performance’, EP), which covers the ability to effectively perform the maneuvers as intended (Table 1). The five items of each dimension are rated dichotomously (0 = no, 1 = yes) and summed to yield a score for the RI (ACSID-RI, range 0–5) and the EP dimension (ACSID-EP, range 0–5). A total score is calculated as the sum of both dimension scores (ACSID-T, range 0–10). The ACSID has been shown to have good-to-excellent inter-/intra-rater reliability, concurrent validity, and feasibility, and to be sensitive to intervention-induced changes in patients with mild-to-moderate dementia [62].

Table 1

Scoring guide for the Assessment of Compensatory Sit-to-stand Maneuvers in People with Dementia [62]

STS maneuver/ACSID Item	Dimension	Description of Scoring
(1) Buttocks displacement	RI	0 pt.	No buttocks displacement
		1 pt.	Deliberate buttocks displacement (anterior or posterior) on the chair seat
	EP	0 pt.	Buttocks placed in the posterior portion of the chair seat
		1 pt.	Buttocks placed in the anterior portion of the chair seat (≥center of the seat)
(2) Feet displacement	RI	0 pt.	No feet displacement
		1 pt.	Deliberate feet displacement (anterior or posterior)
	EP	0 pt.	Anterior feet position, toes in front of the knees
		1 pt.	Posterior feet position, toes behind or aligned with the knees
(3) Trunk straightening	RI	0 pt.	No change of upper body posture
		1 pt.	Straightening the upper body to an extended active sitting posture (e.g., by raising up the chest, pulling shoulders back, anterior tilting of the pelvis)
	EP	0 pt.	Relaxed passive (slump) upper body posture during trunk flexion (increased thoracic kyphosis and posterior pelvic tilt)
		1 pt.	Extended active upper body posture during trunk flexion (upper trunk extension while the lower trunk rotates forward at the hips)
(4) Trunk flexion	RI	0 pt.	No excessive trunk flexion
		1 pt.	Excessive trunk flexion prior or after the moment at which the buttocks begins to leave the chair seat (lift-off)
	EP	0 pt.	No excessive trunk flexion
		1 pt.	Excessive trunk flexion prior to lift-off
(5) Standing up	RI	0 pt.	No attempt to raise
		1 pt.	Obvious attempt to raise (buttocks starts leaving contact with the chair)
	EP	0 pt.	No upright standing posture (flexed knee and/or hip joints)
		1 pt.	upright standing posture (knee and hip joints as fully extended as possible)
ACSID-RI score		0–5 pt.
ACSID-EP score		0–5 pt.
ACSID total score		0–10 pt.

STS, sit-to-stand; ACSID, Assessment of Compensatory Sit-to-stand Maneuvers in People with Dementia; RI, recall and initiation; EP, effective performance; pt, points.

Body-fixed-sensor-based STS analysis

The STS transfers were additionally analyzed using a small and light (87×45×14 mm, 74 grams) body-fixed sensor (BFS) system (DynaPort^® Hybrid, McRoberts, The Hague, The Netherlands), which was inserted in an elastic belt fixed around the waist close to the center of mass. The BFS system contains three pre-calibrated accelerometers (STM-LIS3LV02DQ) and three gyroscopes (EPSON-XV-3500CB) and measures 3-dimensional accelerations and angular velocities of the trunk at a sampling rate of 100 Hz. The online analysis software of the BFS system allows an automatic analysis of the temporal and kinematic motion parameters of different phases (sit-to-stand and stand-to-sit) and sub-phases (flexion and extension) during repeated STS transfers. The BFS-based STS analysis has been demonstrated to be feasible, valid and reliable in geriatric settings [63 –65]. The BFS outcome parameters used in this study were range of the STS trunk flexion angle, duration and maximum angular velocity of the STS trunk flexion, and duration of the STS movement phase. The STS movement strategy trained in the motor learning exercise program was characterized by slow consecutive movement maneuvers during the STS movement phase, including a slow, excessive trunk flexion before rising from the chair and extending the trunk and the knees in order to reach an upright standing position. According to these motion characteristics, we hypothesized that learning to integrate the compensatory STS maneuvers into the STS transfer will be associated with an increase of the trunk flexion range, trunk flexion duration and STS movement duration, and with a decrease of the maximum trunk flexion angular velocity.

Procedure

The test procedure was conducted according to a standardized written test protocol. Initially, the belt with the BFS system was attached on the participants’ lower back at the height of the second lumbar vertebra. The participants were seated on an armless, backless chair of adjustable height, with seat placed at 100% knee height, measured as the distance from the left medial tibial plateau to the floor [18]. At baseline, participants were first asked to perform a single chair stand test without using their arms in order to assess the general STS ability [66]. If participants were unable to stand up from the regular seat height due to physical limitations, the seat was adjusted to 110% (120%) of knee height [65]. This seat height was used for further procedure at baseline, and for the post-intervention and follow-up assessments. On a standard chair placed in the sagittal plane in front of the seated participant, the test administrator initially demonstrated the compensatory STS movement strategy for one time at all assessment sessions (T1, T2, and T3). Each movement maneuver of the strategy was simultaneously accompanied by a standardized verbal cue given by the administrator during the demonstration: (1) ‘slide forward to the front edge of the chair seat’; (2) ‘move the feet backwards to the edge of the chair seat’; (3) ‘straighten the upper body, erect the back, and raise up the chest’; (4) ‘bend the upper body forwards until your buttocks starts leaving the chair seat’; and (5) ‘raise up in an upright standing position without using your arms.’ Immediately after the demonstration, the participant was instructed to stand up 5 times in a row applying the movement strategy demonstrated before (‘arise from the chair 5 times in the way it was demonstrated before’). No instructions were given on the speed of standing up. Repeated chair stands could be performed at self-selected pace with short breaks between chair stands if needed (e.g., due to physical limitations or the need for reflection time). The buttocks and foot placement were not standardized. Each participant was allowed to relax into his/her own comfortable initial sitting position. During testing, no physical or cognitive assistance was allowed. Each compensatory STS transfer was simultaneously videotaped by a digital camcorder (Xacti VPC-FH1, SANYO Electric Co Ltd, Moriguchi, Japan), positioned perpendicular to the left sagittal plane of the participant. Video and BFS data were collected from initial sitting to the final standing position at the end of the fifth stand. The video recordings were used for the ACSID scoring by a trained rater blinded to the participants’ group allocation. The BFS raw data stored on a Micro-SD card were uploaded to the online analysis software for automatic STS analysis.

Statistical analysis

Descriptive data were presented as frequencies and percentages for categorical variables, and means and standard deviations or medians and ranges for continuous variables as appropriate. Unpaired t-tests, Mann-Whitney U-tests, and Chi-square tests were used for baseline comparison according to the data distribution. Primary outcomes were the observation-based ACSID scores, and secondary outcomes were the BFS-recorded data. For the statistical analysis of the ACSID scores, we used the STS trial with the highest ACSID-T score [62]. The BFS outcomes were analyzed based on mean values of the different STS trials [65]. Between-group changes over the intervention period (T1-T2) and the total observation period (T1-T3) were analyzed by two-way analyses of variance for repeated measures (repeated measures ANOVA, group×time). Effect sizes for intervention effects were calculated as partial eta squared (η _p ²). Partial eta squared values were interpreted as small (η_p² < 0.06), medium (0.06≥η _p ² < 0.14), or large effects (η _p ²≥0.14) [67]. A two-sided p-value of ≤0.05 indicated statistical significance. Statistical analysis was performed on an intention-to-treat basis using IBM SPSS Statistics for Windows, Version 23.0 (IBM Corp., Armonk, NY, USA).

RESULTS

Participant characteristics

Out of 2,876 persons screened for eligibility, 97 were enrolled and randomly assigned to the IG (n = 51) and CG (n = 46). The attrition rate was 15% at T2 (IG: 22%; CG: 9%, p = 0.080) and 27% at T3 (IG: 27%; CG: 26%, p = 0.880) (Fig. 1). No major health problems occurred during training or testing. All serious medical events and causes of death were related to pre-existing comorbidity, and none were directly or indirectly attributable to the exercise program. Twelve participants dropped out due to serious medical events (n = 8) or death (n = 4); another 12 interrupted training and rejected any additional testing, despite repeated efforts of persuasion, and 5 had to be excluded from assessment due to severe physical limitations and pain. One participant rejected the post-intervention assessment but was willing and able to be tested at the 3-month follow-up assessment.

Fig.1

Flow chart for screening, recruitment, allocation, intervention, follow-up, and data analysis.

The study sample comprised multimorbid, frail older people with mild-to-moderate dementia. Participants’ mean age was 82.5±5.9 y and the mean MMSE score was 21.9±2.9 points. Physical performance was impaired: the POMA score averaged 22.4±4.0 points, the TUG time averaged 18.2±11.1 s, and thirty-six participants (37.1%) were not able to rise from a chair with seat at individual knee height without using arms. Almost half of the participants (n = 46 [47.4%]) reported one or more falls in the previous year. Sixty-five participants (67.0%) were living independently at home, partly with supportive care; 32 (33.0%) were institutionalized. Descriptive variables (p = 0.196–0.942) and outcome measures (p = 0.250–0.960) at baseline did not differ significantly between the IG and CG (Table 2), indicating a successful randomization. When dropouts (n = 26) were compared with those participants who stayed in the study until the end of follow-up (n = 71), no significant differences were found for any baseline variable (p = 0.092–0.903). Dropout-adjusted groups did not differ significantly in any descriptive variables (p = 0.126–0.990) or outcome measures at baseline (p = 0.204–0.734). Results are consistent with the statistical analysis for the total sample initially recruited, indicating that both groups were still comparable despite missing measures.

Table 2

Participants’ characteristics for the intervention group (IG) and control group (CG)

Variable	IG (n = 51)	CG (n = 46)	p-value
Age, years, mean±SD^a	82.6±6.1	82.5±5.7	0.887
Gender, female, n (%)^b	36 (70.6)	36 (78.3)	0.388
Mini-Mental State Examination, score, mean±SD^a	22.2±2.9	21.5±3.0	0.214
Education, years, median (range)^c	11 (7–20)	11 (7–19)	0.760
Number of diagnoses, mean±SD^a	7.8±4.0	8.8±4.6	0.265
Number of medications, mean±SD^a	7.5±3.5	7.7±3.4	0.812
Taking cholinesterase inhibitors and/or memantine, n (%)^b	39 (76.5)	29 (63.0)	0.149
Performance Oriented Mobility Assessment, score, mean±SD^a	22.6±4.2	22.2±3.8	0.629
Timed Up and Go, s, median (range)^c	14.3 (6.5–51.2)	15.1 (8.0–86.0)	0.942
Single chair stand test, n (%)^b	29 (47.5)	32 (52.5)	0.196
Geriatric Depression Scale, score, mean±SD^a	2.8±2.2	2.8±2.4	0.898
Falls Efficacy Scale International (short version), score, median (range)^c	8 (7–18)	8 (7–16)	0.445
Recent history of falls, n (%)^b	20 (39.2)	26 (56.5)	0.088
12-item Short Form Health Survey, score, mean±SD^a
Physical component summary	44.3±9.5	45.5±8.7	0.549
Mental component summary	49.6±7.5	49.9±8.3	0.872
Living situation, n (%)^b			0.430
Community-dwelling	36 (70.6)	29 (63.0)
Institutionalized	15 (29.4)	17 (37.0)

p-values are given for ^at-tests, ^bChi-square tests, and ^cMann-Whitney U-tests applied to test for differences between the intervention and control group.

The standardized, automated analysis of BFS raw data by using the online software failed in 8 measurements (T1: n = 3, T2: n = 2, T3: n = 3; overall: 2.8% of measurements), which reduced the sample size for the BFS-based outcomes.

Effects of intervention

Adherence to the intervention was excellent in both groups, averaging 98.1±3.7% in the IG and 96.5±6.5% in the CG, with no significant difference between groups (p = 0.178). The primary hypothesis was verified by significant improvements (p < 0.001) in the IG compared to the CG in all ACSID scores, with overall large effect sizes (η _p ² = 0.261–0.372) (Table 3). These results were confirmed by the secondary outcomes with significant positive changes (p < 0.001–0.006) in the IG compared to the CG in all BFS-based outcomes. Effect sizes for BFS-based outcomes were between medium and large (η _p ² = 0.099–0.188).

Table 3

Effects of the intervention: STS measurements before the intervention (T1), at the end of the 10-week intervention (T2), and at follow-up 3-month following intervention (T3) for the intervention group (IG) and control group (CG)

	T1		T2		T3		T1–T2			T1–T3
Variable	n	mean±SD	n	mean±SD	n	mean±SD	Δ ^a	p-	effect	Δ ^a	p-	effect
							mean±SD	value^b	size^c	mean±SD	value^b	size^c
Primary outcomes
ACSID recall and initiation, score
IG	48	1.8±1.0	40	3.3±1.3	37	2.5±1.2	+1.7±1.7	<0.001	0.319	+0.9±1.3	0.015	0.084
CG	46	1.8±1.0	42	1.7±0.9	34	2.0±1.0	–0.1±0.9			+0.2±1.1
ACSID effective performance, score
IG	48	2.1±0.9	40	3.1±1.0	37	2.6±1.1	+1.0±0.9	<0.001	0.261	+0.5±1.3	0.118	0.036
CG	46	1.9±0.9	42	1.8±0.8	34	2.1±1.0	–0.1±0.9			+0.2±1.1
ACSID total, score
IG	48	3.9±1.4	40	6.4±2.1	37	5.1±2.1	+2.7±2.2	<0.001	0.372	+1.4±2.1	0.012	0.090
CG	46	3.7±1.4	42	3.5±1.5	34	4.1±1.6	–0.1±1.4			+0.3±1.5
Secondary outcomes
Trunk flexion range, °
IG	45	33.58±7.52	39	40.23±12.84	35	38.93±12.84	+8.28±13.41	0.006	0.099	+4.91±11.72	0.147	0.033
CG	46	33.08±9.90	41	34.87±10.51	33	36.14±11.11	+0.91±8.95			+0.97±9.87
Trunk flexion duration, s
IG	45	1.20±0.92	39	1.84±1.11	35	1.57±1.00	+0.81±1.24	<0.001	0.188	+0.40±0.90	0.020	0.083
CG	46	1.14±0.52	41	1.06±0.49	33	1.17±0.58	–0.10±0.61			–0.05±0.59
Maximum trunk flexion angular velocity, °/s
IG	45	78.98±27.44	39	64.82±27.14	35	73.78±26.10	–12.34±26.44	0.002	0.127	–5.44±29.36	0.093	0.044
CG	46	73.89±26.61	41	81.44±26.78	33	82.51±28.11	+5.87±22.00			+5.47±21.86
STS movement duration, s
IG	45	2.10±1.10	39	2.84±1.35	35	2.57±1.26	+0.94±1.47	<0.001	0.158	+0.53±1.15	0.018	0.086
CG	46	2.11±0.88	41	2.00±0.73	33	2.09±0.90	–0.10±0.93			–0.09±0.91

SD, standard deviation; ACSID, Assessment of Compensatory Sit-to-stand Maneuvers in People with Dementia; s, seconds; °, degrees; °/s, degrees per seconds; STS, sit-to-stand; STS movement duration was defined as the time from the start of the trunk flexion in the sitting position to the end of the trunk extension in the standing position; ^aΔ, absolute change, calculated as: (retest score –baseline score); ^bp-values are given for group×time interaction effect as calculated by 2-way analysis of variance for repeated measures; ^cEffect sizes are given as partial eta squared η _p ² for group×time interaction. Increase in ACSID scores, trunk flexion range/duration, and STS movement duration and decrease in maximum trunk flexion angular velocity indicate learning.

Sustainability of effects

The learning gains of the IG compared to the CG decreased in the follow up, but effects were sustained for those primary and secondary outcomes that showed the largest effects sizes from baseline to post-intervention assessment (Table 3). Three months after training completion, the ACSID-RI (p = 0.015) and ACSID-T scores (p = 0.012) remained elevated with significant differences between IG and CG. The ACSID-EP score was also still increased in the IG (time effect for T1 versus T3 : 2.1±0.9 versus 2.6±1.1 points, p = 0.016, η_p² = 0.154), but between-group differences over time were no longer significant (group×time effect for T1 versus T3: p = 0.118, η_p² = 0.036). In the BFS-based outcomes, improvements of the IG compared to the CG were sustained for the STS movement duration (p = 0.019, η_p² = 0.086) and the duration of the STS trunk flexion (p = 0.020, η_p² = 0.083). The range of the STS trunk flexion was also still improved in the IG (time effect for T1 versus T3 : 33.53±6.37 versus 38.44±12.39 degrees, p = 0.024, η_p² = 0.154), but between-group differences over time disappeared (group×time effect for T1 versus T3: p = 0.093–0.144, η _p ² = 0.034–0.044). The improvements in the maximum trunk flexion angular velocity angle were not sustained.

DISCUSSION

The presented randomized controlled trial demonstrated that the motor learning exercise program specifically designed for the target sample of cognitively impaired individuals was effective in teaching compensatory STS maneuvers to people with mild-to-moderate dementia. To the best of our knowledge, this is the first study showing that PwD can learn and retain movement maneuvers for a complex motor skill highly relevant to everyday life.

Effects of intervention

Training-induced improvements of the IG in all ACSID scores confirmed the primary study hypothesis that PwD can learn compensatory STS maneuvers. The increased score observed for the cognitive dimension (ACSID-RI) reflects the ability of the IG participants to consciously recollect and initiate an increased number of movement maneuvers in response to the dementia-specific motor learning exercise program. This finding is in contrast to the results reported in the study by Rösler et al. [8], which has been the only study so far that examined motor learning in dementia by using a complex gross motor skill, namely waltz dancing. In this study, patients with moderate dementia showed improved rhythmicity, expression, smoothness of movement, creativity and usage of space after a 12-day dance-exercise program on a slow-waltz (to be danced alone); however, they were not able to explicitly recollect new dance steps after the intervention period. This might be due to the fact that the exercise program used in this study seems not to have been specifically designed for PwD. By applying teaching methods and practice conditions that have been demonstrated to be effective in (re-)learning of other motor or everyday tasks in PwD [7, 41], and following the recommendations given for physical exercise practice in PwD [48], the presented study showed for the first time that PwD can successfully recollect movement maneuvers for a complex gross motor task when a dementia-specific motor learning exercise program was used.

The score for the motor dimension (ACSID-EP) was also found to be increased in the IG participants at post-intervention, indicating that they learned to effectively perform an increased number of recollected movement maneuvers. Although PwD may lose their capacity of preparing and executing efficient body motions [26 , 29], this result suggests that PwD can (re-)learn to effectively integrate high-level, cognitive aspects of motor processes into the motor action organization in order to improve the quality and efficiency of motions, which might be crucial in individuals with high risk of falls. Immediate error correction and haptic assistance provided by trainers during the learning process may help to achieve such motor learning effects.

Learning gains were also suggested by overall positive changes in all BFS-recorded, temporal, kinematic STS motion parameters. Training-related change scores in the STS movement duration, the trunk flexion duration, and the maximum trunk flexion angular velocity substantially exceeded the minimal detectable change reported in geriatric patients for these parameters [65], indicating a real, clinically relevant change in the STS movement execution. As the compensatory STS movement strategy was characterized by including individual, slow consecutive movement maneuvers in the STS movement phase, the increased STS movement duration indicates that the IG participants learned to integrate such maneuvers into this movement phase. A more specific indication that supports the primary study hypothesis based on technically measured outcomes was provided by the increased trunk flexion range and trunk flexion duration as well as by the decreased maximum trunk flexion angular velocity. Given the excessive trunk flexion taught during the motor learning exercise program, this result suggests that IG participants learned to integrate an increased forward trunk flexion into the STS transfer. These positive changes in spatiotemporal features of the trunk flexion are of special interest as STS movement disorders in PwD have been associated with a reduced forward trunk flexion coupled with an earlier initiation of motion components in the vertical plane (‘dominant vertical chair-rise strategy’), decreasing the overall STS movement quality and efficiency [18, 26]. Integrating a more pronounced trunk flexion into the STS movement phase shifts the center of mass more toward the rotational axis of the knee joint and the base of support which reduces the knee torque and the muscle strength in lower extremities needed to achieve the standing position thus increases the STS movement efficiency [26, 68].

Overall, our results substantiate findings of previous studies that reported preserved motor learning abilities in PwD by using fine or gross motor tasks without relevance to everyday life [6 –11]. The overall improvements in all our study outcomes demonstrate that PwD were also able to learn movement maneuvers that aim to improve qualitative aspects of a complex gross motor skill, namely the STS transfer, which represents a hallmark of everyday functioning, independence, and quality of life in older adults [66, 69].

Sustainability of learning effects

Motor learning is defined as ‘a set of processes associated with practice or experience leading to relatively permanent changes in the capability for skilled movement’ ([50], p. 327). To evaluate a ‘relatively permanent change’ in motor behavior, it is essential to include long-term follow-up assessments in the research design of studies on motor learning. Previous studies on motor learning in PwD, however, often lack long-term follow-up [6 , 13–16]. Of the few studies that have investigated and found preserved long-term retention of motor learning in PwD, all have used experimental motor tasks with no direct relevance to patients’ everyday life [12 , 71]. For the first time, our results suggest that, for at least three months following training, PwD were also able to retain some movement maneuvers for a complex motor skill highly relevant to everyday functioning. As would be expected, the learning gains waned after training cessation; however, significant, training-induced improvements remained at the end of the follow-up period for most of the outcomes. Learning effects were sustained for the primary and the secondary outcomes that had the largest effect sizes during training, indicating sustainability of the dementia-specific motor learning exercise program despite the progressive nature of participants’ cognitive impairment.

Feasibility, adherence, and safety

Based on the patient-centered approach, the dropout rate in the present study after the intervention period (15%) was lower those that reported in some other previous studies (about 20–36%) performing a physical exercise program in PwD with similar intervention length (8–12 weeks), frequency (2–3 times a week), and session duration (45–120 min) [72 –76]. Training adherence was excellent in both study groups (97%). According to previous studies [72, 77], these results indicate that a high training adherence (>90%) can be achieved by a physical exercise program specifically designed for PwD, despite participants’ multimorbidity, poor functional status, and advanced cognitive impairment. Participants’ safety was a clear focus in this study as the intervention was strictly supervised by qualified trainers and specifically adjusted to the needs and abilities of PwD. As a result, no severe training-related adverse events occurred in the highly challenging sample of multimorbid, frail older PwD.

Limitations and future research

Although we performed a highly task-specific motor learning exercise program on compensatory STS maneuvers and used an assessment strategy specifically developed to document the specific intervention effects of this training component, we cannot exclude a relative, non-specific contribution of the additional training components (i.e., walking while counting, exergaming) to the learning gains observed in the IG due to the study design. Another limitation of this study is that our results achieved in patients with mild-to-moderate dementia may not be generalizable to PwD in a more advanced disease stage, with severe cognitive impairment or inability to rise from a chair. Further studies are needed to examine such hypotheses. It remains also a future research question whether PwD are able to integrate successfully learned compensatory STS maneuvers into their daily-life STS movement execution. STS motion parameters measured under controlled and standardized conditions may differ significantly from those measured under daily-life conditions, and thus may only provide an optimistic estimate on how a person actually performs the STS motion in daily life [78]. In future studies, the use of wearable motion sensors for long-term physical activity monitoring may allow the analysis of potential training-induced changes in temporal and kinematic STS motion parameters (e.g., STS duration, acceleration, angular velocity) also in the participants’ home environment during daily life as well as the analysis of potential differences between the STS motion measured in daily life and that measured in a standardized test scenario.

Conclusion

The presented study clearly demonstrated that the dementia-specific motor learning exercise program was feasible and enabled multimorbid, frail older people with mild-to-moderate dementia to learn and retain the compensatory STS maneuvers commonly taught in geriatric rehabilitation therapy to enhance a patient’s STS ability. To the best of our knowledge, this is the first study that revealed preserved motor learning abilities in PwD by use of a complex motor skill with direct relevant to everyday life. The study provides insight as to how such motor skills can be taught effectively in PwD. The teaching methods and practice conditions used in the presented motor learning exercise program may help to establish specifically designed rehabilitation or outpatient exercise programs for PwD that focus on (re-)learning clinically relevant motor tasks, or improving qualitative aspects in their movement execution, in order to reduce patients’ risk of falling and to preserve or promote their mobility and functional independence.

Footnotes

ACKNOWLEDGMENTS

We kindly thank Michaela Günther-Lange (Agaplesion Bethanien Hospital Heidelberg, Geriatric Center at the University of Heidelberg) for her assistance in training and supervision of participants.

The study was supported by the Dietmar Hopp Foundation, the Robert Bosch Foundation, and the Network of Aging Research (NAR) at the University of Heidelberg. The sponsors had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript.

Authors’ disclosures available online ().

References

Magill

(2011) Motor learning and control: Concepts and applications, McGraw-Hill, New York, NY.

Muratori

, Lamberg

, Quinn

, Duff

(2013) Applying principles of motor learning and control to upper extremity rehabilitation. J Hand Ther 26, 94–103.

Sadeghi

, Minor

, Cullen

(2010) Neural correlates of motor learning in the vestibulo-ocular reflex: Dynamic regulation of multimodal integration in the macaque vestibular system. J Neurosci 30, 10158–10168.

Ren

, Wu

, Chan

, Yan

(2013) Cognitive aging affects motor performance and learning. Geriatr Gerontol Int 13, 19–27.

, Chan

, Yan

(2016) Mild cognitive impairment affects motor control and skill learning. Rev Neurosci 27, 197–217.

Yan

, Abernethy

, Li

(2010) The effects of ageing and cognitive impairment on on-line and off-line motor learning. Appl Cognit Psychol 24, 200–212.

van

Halteren-van Tilborg IA

, Scherder

, Hulstijn

(2007) Motor-skill learning in Alzheimer’s disease: A review with an eye to the clinical practice. Neuropsychol Rev 17, 203–212.

Rösler

, Seifritz

, Krauchi

, Spoerl

, Brokuslaus

, Proserpi

, Gendre

, Savaskan

, Hofmann

(2002) Skill learning in patients with moderate Alzheimer’s disease: A prospective pilot-study of waltz-lessons. Int J Geriatr Psychiatry 17, 1155–1156.

Schmitz

, Bier

, Joubert

, Lejeune

, Salmon

, Rouleau

, Meulemans

(2014) The benefits of errorless learning for serial reaction time performance in Alzheimer’s disease. J Alzheimers Dis 39, 287–300.

10.

van

Tilborg I

, Hulstijn

(2010) Implicit motor learning in patients with Parkinson’s and Alzheimer’s disease: Differences in learning abilities? Motor Control 14, 344–361.

11.

Yan

, Dick

(2006) Practice effects on motor control in healthy seniors and patients with mild cognitive impairment and Alzheimer’s disease. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 13, 385–410.

12.

Dick

, Shankle

, Beth

, Dick-Muehlke

, Cotman

, Kean

(1996) Acquisition and long-term retention of a gross motor skill in Alzheimer’s disease patients under constant and varied practice conditions., P. J Gerontol B Psychol Sci Soc Sci 51, 103–111.

13.

Dick

, Andel

, Hsieh

, Bricker

, Davis

, Dick-Muehlke

(2000) Contextual interference and motor skill learning in Alzheimer’s disease. Aging Neuropsychol Cogn 7, 273–287.

14.

Dick

, Hsieh

, Dick-Muehlke

, Davis

, Cotman

(2000) The variability of practice hypothesis in motor learning: Does it apply to Alzheimer’s disease? Brain Cogn 44, 470–489.

15.

Dick

, Hsieh

, Bricker

, Dick-Muehlke

(2003) Facilitating acquisition and transfer of a continuous motor task in healthy older adults and patients with Alzheimer’s disease. Neuropsychology 17, 202–212.

16.

Willingham

, Peterson

, Manning

, Brashear

(1997) Patients with Alzheimer’s disease who cannot perform some motor skills show normal learning of other motor skills. Neuropsychology 11, 261–271.

17.

Lindemann

, Muche

, Stuber

, Zijlstra

, Hauer

, Becker

(2007) Coordination of strength exertion during the chair-rise movement in very old people. J Gerontol A Biol Sci Med Sci 62, 636–640.

18.

Scarborough

, Krebs

, Harris

(1999) Quadriceps muscle strength and dynamic stability in elderly persons. Gait Posture 10, 10–20.

19.

Schenkman

, Hughes

, Samsa

, Studenski

(1996) The relative importance of strength and balance in chair rise by functionally impaired older individuals. J Am Geriatr Soc 44, 1441–1446.

20.

Alexander

(1994) Postural control in older adults. J Am Geriatr Soc 42, 93–108.

21.

Ferrucci

, Cooper

, Shardell

, Simonsick

, Schrack

, Kuh

(2016) Age-related change in mobility: Perspectives from life course epidemiology and geroscience. J Gerontol A Biol Sci Med Sci 71, 1184–1194.

22.

Whipple

, Wolfson

, Derby

, Singh

, Tobin

(1993) Altered sensory function and balance in older persons. (Spec No). J Gerontol 48, 71–76.

23.

Tinetti

, Speechley

, Ginter

(1988) Risk factors for falls among elderly persons living in the community. N Engl J Med 319, 1701–1707.

24.

Williamson

, Fried

(1996) Characterization of older adults who attribute functional decrements to “old age”. J Am Geriatr Soc 44, 1429–1434.

25.

Rapp

, Becker

, Cameron

, Konig

, Buchele

(2012) Epidemiology of falls in residential aged care: Analysis of more than 70,000 falls from residents of bavarian nursing homes., 187.e. J Am Med Dir Assoc 13, 1–6.

26.

Manckoundia

, Mourey

, Pfitzenmeyer

, Papaxanthis

(2006) Comon of motor strategies in sit-to-stand and back-to-sit motions between healthy and Alzheimer’s disease elderly subjects. Neuroscience 137, 385–392 paris.

27.

Perry

, Hodges JR (1999) Attention and executive deficits in Alzheimer’s disease. A critical review. Brain 122, 383–404.

28.

Lezak

, Howieson

, Bigler

, Tranel

(2012) Neuropsychological Assessment, New York, Oxford University Press.

29.

Ghilardi

, Alberoni

, Marelli

, Marina

, Franceschi

, Ghez

, Fazio

(1999) Impaired movement control in Alzheimer’s disease. Neurosci Lett 260, 45–48.

30.

Allan

, Ballard

, Rowan

, Kenny

(2009) Incidence and prediction of falls in dementia: A prospective study in older people. PLoS One 4, e5521.

31.

Barreca

, Sigouin

, Lambert

, Ansley

(2004) Effects of extra training on the ability of stroke survivors to perform an independent sit-to-stand: A randomized controlled trial. J Geriatr Phys Ther 27, 59–68.

32.

Alexander

, Galecki

, Grenier

, Nyquist

, Hofmeyer

, Grunawalt

, Medell

, Fry-Welch

(2001) Task-specific resistance training to improve the ability of activities of daily living-impaired older adults to rise from a bed and from a chair. J Am Geriatr Soc 49, 1418–1427.

33.

Akram

, McIlroy

(2011) Challenging horizontal movement of thebody during sit-to-stand: Impact on stability in the young andelderly. J Mot Behav 43, 147–153.

34.

Khemlani

, Carr

, Crosbie

(1999) Muscle synergies and joint linkages in sit-to-stand under two initial foot positions. Clin Biomech (Bristol, Avon) 14, 236–246.

35.

Fulk

(2010) Interventions to improve transfers and wheelchair skills. In, O’Sullivan SB, Schmitz TJ, eds. F.A. Ds Company, pp. Improving Functional Outcomes in Physical Rehabilitation 138–162

Philadelphia, PA

avi.

36.

Shepherd

, Gentile

(1994) Sit-to-stand: Functional relationship between upper body and lower limb segments. Hum Mov Sci 13, 817–840.

37.

Schmidt

(1975) A schema theory of discrete motor skill learning. Psychol Rev 82, 225–260.

38.

Magill

, Hall

(1990) A review of the contextual interference effect in motor skill acquisition. Hum Mov Sci 9, 241–289.

39.

Schöllhorn

(1999) Individualität - ein vernachlässigter Parameter? Leistungssport 29, 5–12.

40.

Clare

, Jones

(2008) Errorless learning in the rehabilitation of memory impairment: A critical review. Neuropsychol Rev 18, 1–23.

41.

Werd MM

, Boelen

, Rikkert

, Kessels

(2013) Errorless learning of everyday tasks in people with dementia. Clin Interv Aging 8, 1177–1190.

42.

Folstein

, Folstein

, McHugh

(1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189–198.

43.

Morris

, Mohs

, Rogers

, Fillenbaum

, Heyman

(1988) Consortium to establish a registry for Alzheimer’s disease (CERAD) clinical and neuropsychological assessment of Alzheimer’s disease. Psychopharmacol Bull 24, 641–652.

44.

Oswald

, Fleischmann

(1999) Das Nürnberger Alters-Inventar (NAI) -NAI-Testmanual und Textband, Hogrefe, Göttingen.

45.

Belle

, Mendelsohn

, Seaberg

, Ratcliff

(2000) A brief cognitive screening battery for dementia in the community. Neuroepidemiology 19, 43–50.

46.

Aebi

(2002) Validierung der Neuropsychologischen Testbatterie CERAD-NP. Eine Multi-Center Studie, PhD Thesis, University of Basel, Switzerland.

47.

Wei

L-J

(1977) A class of designs for sequential clinical trials. J Am Stat Assoc 72, 382–386.

48.

Oddy

(1987) Promoting mobility in patients with dementia: Some suggested strategies for physiotherapists. Physiother Pract 3, 18–27.

49.

Schwenk

, Oster

, Hauer

(2008) Kraft- und Funktionstraining bei älteren Menschen mit demetieller Erkrankung. Praxis Physiotherapie 2, 59–65.

50.

Schmidt

, Lee

(2005) Motor control and learning: A behavioral emphasis, Human Kinetics, Champaign, IL.

51.

Eberspächer

(2012) Mentales Training - Das Handbuch für Training und Sportler, Copress Sport, Munich, Germany.

52.

Landin

(1994) The role of verbal cues in skill learning. }. Quest 46, 299–313.

53.

Glisky

, Schacter

, Tulving

(1986) Learning and retention of computer-related vocabulary in memory-impaired patients: Method of vanishing cues. J Clin Exp Neuropsychol 8, 292–312.

54.

O’Sullivan

(2010) Interventions to improve motor control and motor learning. In Improving Functional Outcomes in Physical Rehabilitation, O’Sullivan

, Schmitz

, eds. F.A. Davis Company, Philadelphia, pp. 12–41.

55.

Kitwood

, Bredin

(1992) Towards a theory of dementia care: Personhood and well-being. Ageing Soc 12, 269–287.

56.

Gauggel

, Birkner

(1999) Validität und Reliabilität einer deutschen Version der Geriatrischen Depressionsskala (GDS). Z Klin Psychol Psychother 28, 18–27.

57.

Ware

Jr. , Kosinski

, Keller

(1996) A 12-Item Short-Form Health Survey: Construction of scales and preliminary tests of reliability and validity. Med Care 34, 220–233.

58.

Hauer

, Kempen

, Schwenk

, Yardley

, Beyer

, Todd

, Oster

, Zijlstra

(2011) Validity and sensitivity to change of the falls efficacy scales international to assess fear of falling in older adults with and without cognitive impairment. Gerontology 57, 462–472.

59.

Tinetti

(1986) Performance-oriented assessment of mobility problems in elderly patients. J Am Geriatr Soc 34, 119–126.

60.

Podsiadlo

, Richardson

(1991) The timed “Up & Go”: A test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39, 142–148.

61.

Hauer

, Oster

(2008) Measuring functional performance in persons with dementia. J Am Geriatr Soc 56, 949–950.

62.

Werner

, Wiloth

, Lemke

, Kronbach

, Hauer

(2016) Development and validation of a novel motor-cognitive assessment strategy of compensatory sit-to-stand maneuvers in people with dementia. J Geriatr Phys Ther. doi: 10.1519/JPT.0000000000000116

63.

van Lummel

, Ainsworth

, Hausdorff

, Lindemann

, Beek

, van Dieen

(2012) Validation of seat-off and seat-on in repeated sit-to-stand movements using a single-body-fixed sensor. Physiol Meas 33, 1855–1867.

64.

Zijlstra

, Mancini

, Lindemann

, Chiari

, Zijlstra

(2012) Sit-stand and stand-sit transitions in older adults and patients with Parkinson’s disease: Event detection based on motion sensors versus force plates. J Neuroeng Rehabil 9, 75.

65.

Schwenk

, Gogulla

, Englert

, Czempik

, Hauer

(2012) Test-retest reliability and minimal detectable change of repeatedsit-to-stand analysis using one body fixed sensor in geriatricpatients. Physiol Meas 33, 1931–1946.

66.

Guralnik

, Simonsick

, Ferrucci

, Glynn

, Berkman

, Blazer

, Scherr

, Wallace

(1994) A short physical performance battery assessing lower extremity function: Association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol 49, M85–94.

67.

Cohen

(1988) Statistical power analysis for the behavioral sciences, Routledge, New York.

68.

Schenkman

, Berger

, Riley

, Mann

, Hodge

(1990) Whole-body movements during rising to standing from sitting. Phys Ther 70, 638–648.

69.

Fusco

, Ferrini

, Santoro

, Lo Monaco

, Gambassi

, Cesari

(2012) Physical function and perceived quality of life in older persons. Aging Clin Exp Res 24, 68–73.

70.

Dick

, Nielson

, Beth

, Shankle

, Cotman

(1995) Acquisition and long-term retention of a fine motor skill in Alzheimer’s disease. Brain Cogn 29, 294–306.

71.

Knopman

(1991) Long-term retention of implicitly acquired learning in patients with Alzheimer’s disease. J Clin Exp Neuropsychol 13, 880–894.

72.

Schwenk

, Zieschang

, Englert

, Grewal

, Najafi

, Hauer

(2014) Improvements in gait characteristics after intensive resistance and functional training in people with dementia: A randomised controlled trial. BMC Geriatrics 14, 73.

73.

Binder

(1995) Implementing a structured exercise program for frail nursing home residents with dementia: Issues and challenges. J Aging Phys Act 3, 383–395.

74.

Hwang

, Choi

(2010) The effects of the dance therapy programthrough rhythmic exercise on cognitivememory performance of the elderly withdementia. & }. Physical Education 4, 12–17.

75.

Binder

(2004) A structured resistive training program improves muscle strength and power in elderly persons with dementia. Act Adapt Aging 28, 35–47.

76.

Thurm

, Scharpf

, Liebermann

, Kolassa

, Elbert

, Lüchtenberg

, Woll

, Kolassa

I-T

(2011) Improvement of cognitive function after physical movement training in institutionalized very frail older adults with dementia. GeroPsych 24, 197–208.

77.

Hauer

, Schwenk

, Zieschang

, Essig

, Becker

, Oster

(2012) Physical training improves motor performance in people with dementia: A randomized controlled trial. J Am Geriatr Soc 60, 8–15.

78.

Zhang

, Regterschot

, Geraedts

, Baldus

, Zijlstra

(2017) Chair rise peak power in daily life measured with a pendant sensor associates with mobility, limitation in activities, and frailty in old people. IEEE J Biomed Health Inform 21, 211–217.