Gait stability and variability measures show effects of impaired cognition and dual tasking in frail people

One in three community-dwelling persons over 65 years of age falls at least once a year and this rate increases rapidly with age, and frailty [1]. Gait and balance disorders are suggested to better predict imminent falls than risk factors in other domains such as impaired vision and medication [1, 2]. Therefore, the objective quantification of gait and balance disorders to detect persons who have high risk of falls is of utmost importance, especially in geriatric patients with cognitive decline who have a high tendency to fall.

Age-associated changes in gait characteristics, such as lower walking speed, reduced step length and increased step time have been interpreted as a more cautious, conservative gait pattern adopted to increase gait stability and decrease fall risk [3, 4]. A more conscious gait pattern, however, may require more cognitive control and result in an attention demanding form of locomotion. If walking requires more cognitive control and becomes less automated, it might be more prone to be influenced by concurrent (cognitive) dual tasks. Even in healthy persons, dual tasks have been shown to affect walking performance [5, 6]. With aging or pathologic conditions, gait changes in response to dual tasking might have a destabilizing effect on the gait pattern [7‐9].

There is growing evidence that executive functions, plays an important role in the ability to perform a motor and cognitive task simultaneously in elderly [10‐12]. Particularly in frail elderly and in persons with Alzheimer's disease, performance of a cognitive task during a motor task is reported to be associated with changes in gait stability and increased fall risk [10, 13, 14]. Stability is a significant component of standing balance and walking. A relatively new approach to quantify gait and balance stability is by means of time dependent analyses of variability using measures derived from the theory of stochastic dynamics [13, 15‐17]. In contrast to more conventional measures, (e.g. mean stride time, walking velocity), which in the case of cyclic movements treat each cycle as being an independent event unrelated to previous or subsequent strides, the applied methods assess fluctuations throughout the gait cycle, and as such provide insight into how behaviour unfolds, taking into account previous states of the system (e.g., cycle trajectory). Applying more traditional measures may mask the temporal variations of the gait pattern due to averaging procedures. A variety of dynamic measures has been used to quantify these time dependent variations in gait patterns, including Detrended Fluctuations Analysis [17], Sample Entropy [18], and Lyapunov exponents [19]. Although conceptually different, these measures assume that walking ability is reflected in dynamic characteristics, in terms of variability in, or local stability of gait patterns. The outcome variables obtained from studies using these methods, have proven to be sensitive to differences between various patient groups and between conditions and are suggested to be related to increased fall risk [4, 9, 19‐22]. Hence, these dynamic parameters may have more power to differentiate between groups and to screen for high risk fallers, particularly in frail elderly whose fall risk might be enhanced by a cognitive impairment. We complemented the stride related measures with measures that quantify time varying patterns of trunk movements during walking and that are closely related to dynamic balance control during walking and standing. The aim of the present study was to examine gait stability and variability of geriatric patients with and without cognitive impairment under normal and dual task walking conditions. Based on previous studies, showing increased stride-to-stride variability during dual tasking and in elderly [4, 14, 22, 23], and in line with the theoretical concept that health is characterized by 'organized' variability, while disease is defined by changes in the structure of variability [24], we hypothesized that dual tasking induced changes in the structure of the variability and decreased local stability of trunk acceleration patterns. Moreover, we anticipated that frail elderly patients with cognitive impairment would be more affected in their capacity to divide attention between a cognitive and a motor task simultaneously, resulting in less stable and more variable gait coordination than cognitive intact frail elderly patients.

The goal of the present study was to assess the effects of dual tasking on gait stability and variability of frail elderly with and without cognitive impairment. We expected that the effect of dual tasking and differences between the cognitive impaired and cognitive intact frail elderly would reveal in the structure of variability of medio-lateral and anterior-posterior trunk accelerations and in stride variability measures, rather than in general velocity and stride time variables.

In general, all participants altered their gait pattern in response to dual tasking by decreasing walking speed and increasing stride time. However, despite lower walking speed, trunk accelerations patterns were more irregular and variable and local stability was decreased in the dual task condition. In addition, stride variability was increased and less structured as quantified by the larger PVI and a decline in the measure α of the DFA. Thus, although the slowing of gait while performing a dual task could reflect an adaptation to more difficult circumstances, the resulting trunk adaptations showed a consistent and therefore statistically significant instability factor, possibly leading to an increased fall risk. These results support the notion that gait is not merely an automated motor activity, but utilizes higher levels of cognitive input, particularly in this population of frail elderly.

Interestingly, no significant differences between the cognitive intact and cognitive impaired elderly were found in gait variables under single task condition. In line with the findings of the study of Toulotte et al.[40], who found differences in gait variables between fallers and non-fallers only in dual task conditions, dual tasking appears to affect walking stronger in de cognitive impaired elderly than in the non-cognitive elderly. This could also explain why over the whole group no significant correlation was observed between the cognitive scores and scores on the test indicative for executive function (clock drawing) and gait variables. However, within the cognitively impaired group, significant associations between cognitive function and several variability measures were found. Walking speed was strongly related to the MMSE and total SMS scores for the cognitive impaired subject but not for the cognitive intact subjects. Moreover walking speed did not discriminate between cognitively impaired and intact participants. This can be explained by the ceiling effect on the MMSE values for the cognitive intact subjects, that is the MMSE values show very little between subject variation, while between subject variation in walking speed is about similar in both groups. In line with our findings, other studies reported weak associations between executive function and/or attention and gait variables under standard walking conditions, that became stronger when walking while performing a dual task [9, 41, 42]. This association, however, was not observed in healthy subjects. In patients without cognitive impairment however, executive function is found to be independently associated with gait function [42].

So, the relation between cognitive functioning and gait variability becomes more visible when the task is more challenging and with a gait pattern that is already impaired, such as in the frail elderly or in patients with Alzheimer's disease. Simultaneously, executed attention demanding tasks compete for attention. In contrast to healthy young and elderly people, who in such situations give priority to the walking task at the cost of lower performance on the cognitive task [43], the stability and variability of the gait pattern deteriorated for all our patients while the quality of the cognitive task was similar in the sitting and walking condition. It is unclear why our subjects prioritise the cognitive task (no such instructions were given), but the same findings have been reported for different patient groups and the favour of one activity over the other might depend on task complexity [7, 44].

In line with previous studies, we found that measures of stride variability and consistency were more sensitive to detect gait changes due to dual tasking than more global gait measures such as gait speed [9, 44]. We complemented these stride related measures with trunk measures that are closely related to dynamic balance control during walking and standing. Presumably, the stability and the pattern of variability of the trunk movements is indicative of the adaptability and the ability to react adequately to withstand small perturbations [7, 16]. The results signify that a more detailed knowledge on gait coordination acquired from this type of analyses might help to identify those who are able to adapt walking ability and those who are not and are thus at greater risk for falls.

Clinically, fall risk is currently quantified mainly by counting the number of falls over a specific time span, for example by using a fall-diary. However, this is a time consuming method and has proven to be not reliable especially in patients who are forgetful [45]. Moreover, falling is an extreme symptom of loss of balance, and one would like to detect the risk of falling in an earlier phase. Although no direct clinical conclusions can be drawn with respect to the detection of falls, our results point out that a combination of accelerometry and off-line dynamical analysis to quantify stride as well as trunk variability and stability provides an objective instrument for screening persons at high risk. Hence, it can be a diagnostic tool for the clinician to examine gait ability and associated fall-risk. Notwithstanding the immediate benefits of accelerometric systems for clinical purposes (i.e., compact and easy-to-use, the subject's minimal awareness of the measuring process on the part of the subject), they also have several drawbacks such as the need to pre-process the data, and the translation to clinically applicable outcome measures. These processes are being automated and simplified for clinical use.

A limitation of the present study is that the groups were small. We nevertheless found significant differences due to dual tasking and between groups. Furthermore, the cognitive intact elderly of our study attended the diagnostic geriatric outpatient clinic for multiple problems, and used multiple medications. Therefore, we did apply a post-hoc analysis with covariate medications but found no significant differential effect between both groups.

In conclusion, the results of the present study provide further support that changes in cognitive functioning are likely to contribute to an increased fall risk, especially in frail elderly when tasks such as walking requires more attention and are combined with concurrent (cognitive) tasks. Walking under dual-task conditions could therefore be helpful when screening individuals with gait impairments and those at risk for falling, as this appears to unmask gait impairments that can provoke falls. We further showed that these impairments can be best discerned by variability and stability measures. When noticing gait instability, future falls might be prevented, by early intervention focusing on fall prevention.