Abstract
Background:
Impairment in gait domains such as pace, rhythm, and variability are associated with falls, cognitive decline, and dementia. However, the longitudinal changes in these gait domains are poorly understood. The aim of this study was to examine age-related changes in gait domains overall and in those with cognitive impairment and mobility disability.
Methods:
Participants were from the LonGenity study (n=797; M Age=75.1 SD 6.5 years; 58.2% female) and were followed up to 12 years (Median=3.3; IQR: 1.1; 6.3). Gait speed and absolute values of step length, step time, cadence and, variability (standard deviation) of step length and step time during usual pace walking were assessed. Principal components analysis was used to obtain weighted combinations of three gait domains: pace (velocity, step length), variability (step length variability, step time variability) and rhythm (step time). Linear mixed effect models were used to examine age-related changes in gait domains overall, and in those with cognitive impairment and mobility disability at baseline.
Results:
Pace declined, and rhythm increased (worsened) in an accelerating non-linear fashion. Variability gradually increased with age. Those with cognitive impairment had faster rates of change in pace and rhythm. Those with mobility disability had faster increases in rhythm.
Conclusions:
Age-related changes in gait domains are not uniform. Individuals with cognitive and mobility impairments are particularly vulnerable to accelerated change in pace and or rhythm.
Keywords: pace, rhythm, variability, cognitive impairments, mobility disability
Introduction
Gait is multifaceted and can be quantified using different spatiotemporal measures [1]. Gait speed is a low-tech and low-cost measure that is associated with multiple clinical outcomes [2]. Other gait characteristics (e.g., step length, double support time variability) can be quantified using footswitches or computerized walkways and are also associated with adverse clinical outcomes, including falls, cognitive decline, and frailty [3–5]. Individual gait measures such as gait speed and step length share considerable covariance. This interdependence between individual gait measures can be exposed with factor analyses, which group individual measures with shared covariance into broader (and uncorrelated) gait domains – such as pace (usually composed of gait speed/velocity and step length), rhythm (composed of time-related gait measures) and variability (composed of intra-individual gait variability in spatiotemporal measures) [1, 6].
Pace, rhythm, and variability are associated with different cognitive functions, subtypes of cognitive impairment, and brain regions. In community-dwelling older adults, pace was associated with decline in global cognition and executive function, non-amnestic MCI and vascular dementia [6, 7], while rhythm was associated with memory decline [6], amnestic MCI, Alzheimer’s disease (AD), and all cause dementia [8, 9]. Slow pace was associated with lower cortical thickness in the anterior cingulate [10] and lower gray matter volume in superior temporal, supplementary motor, and cerebellar regions [11]. By contrast, increased rhythm (poorer performance) was associated with lower cortical thickness in insular and temporal pole regions, and lower gray matter volume in prefrontal cortex, supplementary motor, cingulate and paracingulate regions [10, 11]. Greater variability in individual gait measures have also been associated with smaller cortical thickness in bilateral precentral, inferior frontal, inferior parietal, temporal and lateral occipital regions [12].
Although pace, rhythm and variability domains have been linked to different clinical outcomes and brain regions, no longitudinal studies have examined age-related changes in gait domains – and whether such changes are different in those with cognitive impairment or mobility disability. A better understanding of the relative trajectories of age-related change in gait domains in different populations can assist in designing timely and targeted interventions to prevent late life functional dependence. Therefore, we examined age-related changes in pace, rhythm, and variability in general – and in people with cognitive impairment or mobility disability in particular. We hypothesized that all gait domains would worsen with advancing age and that the rate of change would be specific to each domain. We further examined age-related changes in gait domains as a function of cognitive impairment and mobility disability as these conditions are highly prevalent in aging and accelerate functional decline. We expected that people with these conditions would show accelerated age-related changes in gait domains.
Methods
Study participants
LonGenity study participants who were 65 years and older and had annual assessments for up to 12 years (from 2008 to 2020) were examined. The LonGenity study is an ongoing longitudinal study of older adults of Ashkenazi Jewish decent, that aims to determine the genetic and biological mechanisms of successful aging [13]. Older adults are recruited to the study via public records (i.e., voter registration lists) and community advertising (i.e., newsletters, contacts at synagogues). Participants were defined as offspring of parents with exceptional longevity (OPEL; at least one parent lived ≥95 years) or offspring of parents with usual survival (OPUS). Exclusion criteria include a diagnosis of dementia (>8 on the Blessed Mental Status Examination and >2 on the AD8-item Informant Questionnaire) at initial screening [14], severe visual or hearing impairment, and siblings enrolled in the study. Ethical clearance was obtained from the Committee on Clinical Investigations of Albert Einstein College of Medicine. Written informed consent is obtained from all participants prior to enrollment.
Gait assessment
Gait speed (centimeters/second, cm/s) was measured while participants completed one 8.5-meter walk at their usual pace on a GAITRite® walkway [15]. Participants wore comfortable footwear. The assessments were completed in a quiet, well-lit hallway. To allow for steady pace walking, start and end points were marked 1.2 meters away from both ends of the walkway. Gait speed cadence and average of step length (cm) and step time (s) were directly obtained from the GAITRite® software. The step-to-step fluctuations in gait measures (gait variability) were calculated as the standard deviation (SD) of the respective measure averaged across all footsteps.
Cognitive impairment
Cognitive performance was assessed with a battery of neuropsychological tests including Trail Making Test A and B [16], Digit Span and Digit Symbol Substitution of the Wechsler Adult Intelligence Scale-III (WAIS-III) [17], Boston Naming (15-item) [18], Category and Phonemic fluency tests [19], Figure copy test of the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS) [20], Figure recall test, Free Recall on Free and Cued Selective Reminding Test [21] and Logical Memory of Wechsler Memory Scale-Revised [22]. Cognitive impairment in memory and non-memory related functions was diagnosed by the study neuropsychologist, defined as ≤1.5 SD below age-appropriate cut scores in one or more memory- or non-memory related neuropsychological tests.
Mobility Disability
The United States census of disability statistics defines mobility disability as difficulty in climbing stairs or walking [23]. We adopted subjective difficulty in climbing stairs to identify people with mobility disability (our sample included well-functioning older adults who were able to walk). Difficulty in stair climbing was previously associated with poor medical (hypertension, arthritis), psychological (depression) and sensorimotor (balance, grip strength) factors and was strongly associated with slower stair-climbing time [24].
Covariates
Demographic data (age, sex, marital status, education) and medical history were self-reported. The sum of the dichotomous ratings of presence or absence of 9 medical conditions (hypertension, diabetes, chronic heart failure, arthritis, depression, stroke, chronic obstructive pulmonary disease, myocardial infarction, angina) was calculated to create a global health index. Body mass index (BMI) was calculated using participants’ height (centimeters) and weight (kilograms). A composite measure for global cognition was created from the scores of 11 individual neuropsychological tests as a measure of global cognition [25].
Data analysis
STATA (StataCorp LLC Texas, USA) version 16.1 was used in all the analyses. First, principal component analysis (PCA) was applied to the six baseline gait variables (that represent both spatial and temporal measures and have been associated with poorer outcomes [3, 4, 6]) to derive summary measures for gait domains: pace, rhythm and variability. The purpose of the PCA analysis in this study was to capture the maximum variance in each gait domain while reducing dimensionality (the number of gait measures that were highly correlated), not to interpret the role of each component. Therefore, gait domains were created as the weighted combination of gait measures that were a priori selected based on our prior studies. No rotation was applied [6, 8]. Velocity and step length loaded into the pace domain. Variability in step time and step length loaded into the variability domain. Cadence and step time represented the rhythm domain, but as these measures are the same (cadence=60/step time), for this study rhythm domain was represented with step time. To be consistent with the literature on gait domains we use the term rhythm domain. The same derived components were applied at each wave, to obtain measures for each gait domain at follow up visits.
Longitudinal mixed effect models were used to examine the effect of age (centered age was used as the exposure variable), on the PCA-derived measures of gait domains over time. For all three domains, effects of linear and quadratic terms of centered age were examined. A likelihood ratio test was used to determine the model with the best fit (linear versus non-linear). Effect modifications of the cognitive impairment and mobility disability were tested using an interaction term between these measures with age, in separate models. All models were adjusted for age at baseline, gender, years of education, parental longevity, global health score, BMI, and global cognition at baseline.
Secondary analysis
Previously, different gait domains were associated with different MCI subtypes. Hence, we examined whether rates of change in gait domains are different in people with memory versus non-memory impairment (compared to those without cognitive impairment) using linear mixed effect models.
Results
Table 1 summarizes participant characteristics at baseline. From the initial sample, one participant with dementia at baseline (n=1) and those with missing gait data at baseline (n=298) were excluded leaving a final study sample of 797 older adults (n=705 retained in the study). Supplementary Table 1 summarizes participant characteristics in those who were lost-to-follow-up (n=92) and those who retained (n=705). Those that were lost-to-follow-up were older and had lower education, more people with cognitive impairment, slower gait speed and poorer global cognition test scores. At baseline mean age was 75.1 (SD 6.5), 58.2% (n=464) were female and the median follow-up time was 3.3 (IQR: 1.1–6.3). Supplementary Table 2 summarizes the number of participants and mean age at each follow-up. Table 2 summarizes the proportion of the total variance of each domain explained by the first principal component and the correlation between each domain and the factors loaded into them.
Table 1.
Participant characteristics at baseline
| n=797 | ||
|---|---|---|
| Age (years), mean, SD | 75.1 | 6.5 |
| Female, n, % | 464 | 58.2 |
| Education (years), mean, SD | 17.6 | 2.8 |
| BMI, mean, SD | 27.3 | 4.9 |
| OPEL n, % | 434 | 54.5 |
| Cognitive impairment, n, % | 106 | 13.6 |
| Mobility disability, n, % | 38 | 5.1 |
| Global heath index, n, % | 534 | 67 |
| Gait measure | ||
| Gait speed (cm/s), mean, SD | 110.2 | 20.1 |
| Cognitive measures | ||
| The composite z score for global cognition, mean, SD | 0.8 | 5.4 |
| Digit symbol substitution test, mean, SD | 60.5 | 13.9 |
SD, standard deviation, BMI, body mass index, OPEL, offspring of parents with exceptional longevity, cm, centimeter, s, seconds
Table 2.
Principal component analysis (PCA) loading of independent gait measures into gait domains. Correlations for each gait measure with the domains it is loaded in to and the proportion of the total variance of gait domains explained by the first principal component are shown.
| Pace | Rhythm | Variability | |
|---|---|---|---|
| Velocity | 0.97 | ||
| Step length | 0.97 | ||
| Step time | 0.99 | ||
| Step time variability | 0.94 | ||
| Step length variability | 0.94 | ||
| The proportion of the total variance explained | 0.94 | 0.99 | 0.88 |
Longitudinal changes in gait domains over time
The pace domain showed an accelerating non-linear decline with aging whereas rhythm domain showed an accelerating non-linear increase, after adjusting for baseline age, sex and level of education, parental longevity, BMI, global health score and global cognition(Table 3, Figure 1a). Variability showed a linear increase with aging (Table 3, Figure 1c). Changes in gait domains for both men and women are summarized in Supplementary Table 3.
Table 3.
Changes in gait domains with advancing age
| β (95% CI) at 68.3 years (5thpercentile) | β (95% CI) at 73.4 years (25thpercentile) | β (95% CI) at 78 years (50thpercentile) | β (95% CI) at 83.2 years (75thpercentile) | β (95% CI) at 89.8 years (95thpercentile) | |
|---|---|---|---|---|---|
| Pace | −0.094 (0.110, −0.078) | −0.125 (−0.135, −0.114) | −0.154 (−0.162, −0.146) | −0.187 (−0.198, −0.176) | −0.230 (−0.249, −0.210) |
| Rhythm | 0.002 (0.001, 0.003) | 0.003 (0.002, 0.003) | 0.003 (0.003, 0.004) | 0.004 (0.003, 0.005) | 0.005 (0.004, 0.006) |
| Variability | 0.089 (0.077, 0.101) | ||||
Figure 1.
Changes in pace (top left) rhythm (top right), and variability (bottom panel) with aging. Note: The predicted longitudinal trajectory is based on data with a mean follow up time of 3.9 years
Effect modifications of changes in gait domains by cognitive impairment and mobility disability
Compared to people without cognitive impairment at baseline, those with cognitive impairment showed a faster rate of decline in pace (β= −0.028 95%CI −0.050, −0.006 p=0.014) (Figure 2a) and a faster increase in rhythm (β= 0.001 95%CI 0.0002, 0.002 p=0.018), but not a faster increase in variability (β= 0.006 95%CI −0.015, 0.027, p=0.582). Compared to those without mobility disability at baseline, those with mobility disability had a faster rate of increase in rhythm (β=0.003 95%CI 0.001, 0.005 p=0.004) =0.049 96%CI −0.064, −0.034, p<0.001) (Figure 2b), but not faster decline in pace (β= −0.010 95%CI −0.053, 0.033 p=0.645) or increase in variability (β=−0.011 95%CI −0.051, 0.029 p=0.575).
Figure 2.
Changes in rhythm domain with aging in people with and without the cognitive impairment (top panel) and mobility disability (bottom panel) Note: The predicted longitudinal trajectory is based on data with a mean follow up time of 3.9 years.
Changes in gait domains in different cognitive impairment subtypes
Compared to those without cognitive impairment at baseline, people with non-memory impairment had faster decline in pace while those with memory impairment had faster increase in rhythm (see Supplementary Table 4, Supplementary Figure 1).
Discussion
Impaired gait in aging is a hallmark of declining health. In this sample of community-dwelling older adults without dementia, pace declined, and rhythm (step time) increased in an accelerating non-linear fashion coupled with a linear increase in variability. Individuals with cognitive impairment at baseline showed a faster decline in pace and faster increase in rhythm than those without cognitive impairment. Those with mobility disability at baseline showed a faster increase in rhythm than those without mobility disability. Age-related changes in variability did not differ as a function of cognitive impairment or mobility disability.
Changes in gait domains over time
Prior research suggests that gait domains are associated with different cognitive functions, different types of cognitive impairment, and different brain regions [6, 8–10, 26]. Adding to this knowledge of uniqueness in gait domains, we observed that there are differences in the temporal course of age-related changes in gait domains (e.g., linear versus non-linear trajectories and different rates of change). Both pace and rhythm showed accelerating change (decline and increase, respectively) with aging, however, the rate of change in pace was faster than that of rhythm. A potential explanation for this could be that pace is associated with multiple cognitive functions (e.g. global cognition, executive function) while rhythm is associated with selected cognitive functions (e.g. memory [6]). Pace is also associated with poorer sensorimotor functions (i.e. poorer balance, weaker quadriceps strength) [1], poorer brain structure (smaller cortical thickness and grey matter volume in areas important for cognitive, motor, multisensory integration) [10] and medical conditions that affect multiple brain regions (cardiovascular disease, vascular dementia) [11]. Therefore, the cumulative impairments in many functions may result in a relatively faster decline in pace with advancing age in contrast to rhythm.
In contrast to pace and rhythm, variability showed a linear and gradual increase with advancing age. This suggest that the mechanisms that protect against changes in variability are more robust than those protect against for changes in pace and rhythm. For example, gait variability means lack of consistency in steps. Although in older age, gait is less automatic and steps are more variable, changes in variability could be subtler or more gradual. It is worth reiterating, however, that even if variability shows gradual subtler changes, greater gait variability has been associated with a number of adverse health outcomes, including falls risk and memory decline (even when gait speed showed no association [3, 4, 6]).
Changes in gait domains in people with and without cognitive impairment and mobility disability
Cognitive impairment at baseline modified the trajectories of pace and rhythm such that those with impairment had faster rates of age-related change. In this study, cognitive impairment was defined as worse performance on both memory and non-memory related tasks. It is likely that people with cognitive impairment have pathologies that are widespread across the brain and advanced to a greater degree than those without cognitive impairment, thereby showing faster rates of change in pace and rhythm. Further, in line with our prior studies, we also found that people with memory impairment had faster increase in rhythm whereas those with non-memory impairment had faster decline in pace [8].
Previously, slow gait speed and greater stance time variability were associated with future mobility disability in community-dwelling older adults [27, 28]. In our study, people with mobility disability showed a faster increase in rhythm but did not decline faster in pace or increase faster in variability. Thus, it appears that slower pace and greater variability are more predictive of incident mobility disability, than the presence of mobility disability. Whereas rhythm is directly affected by mobility disability. Collectively, our findings suggest that aging has an overall effect on pace, rhythm, and gait variability. In addition, the slope of decline in pace was modified by cognitive impairment while the slope of increase in rhythm was modified by both cognitive impairment and mobility disability.
Implications of findings and future directions
Impaired performance in pace, rhythm and variability are associated with several but specific adverse health outcomes in older adults [3, 4, 6, 8]. Our study provides novel insights that these gait domains change with advancing age, exposing older adults to a greater risk of declining health. The trajectories of change in different aspects of gait, however, were not uniform. Since different gait domains have been associated with different adverse health outcomes this knowledge offers important information in determining who (at risk) can be identified and around which age. Decline in pace appears to begin early and accelerates in a non-linear fashion with aging. Therefore, slow pace (like gait speed) offers a functional marker that facilitates early identification of at risk older adults, even prior to the age of 65 [25]. Change in variability showed a gradual linear increase. Greater gait variability, however, has been associated with falls and memory decline even when usual pace gait speed showed no associations [3, 4]. Variability has also provided additional information on risk of mobility disability above and beyond that is gait speed [28]. Hence, assessing variability, particularly in specialized falls and memory clinics could provide additional insights into people at risk of poorer health outcomes.
Our purpose in this study was to generate a better understanding of “what happens to gait with advancing age?” by examining the age-associated changes in three important and independent gait domains that have been linked to different adverse clinical outcomes [6–9]. While different gait domains generated from factor analyses provide valuable information on unique gait domains, changes in factors scores can be challenging to use in clinical contexts. Our study findings shows that age-related declines in gait domains are not uniform and differentially associated with cognitive and mobility impairment. To be translated into clinical practice, however, clinically meaningful changes in gait domains need to be established and simple-low cost means to facilitate the assessment of gait domains in clinical settings need to be developed (e.g., smart phone app that can easily calculate measures).
Strengths and limitations
Gait domains provide means to examine different aspects of gait and how gait is related to adverse health outcomes in old age. To the best of our knowledge, this is the first study to examine longitudinal changes in gait domains in aging. We examined whether these changes are linear or non-linear, providing a finer degree of information on longitudinal gait changes. We also examined the impact of cognitive impairment and motor disability on age-related changes in gait domains as people with these conditions are at greater risk of being functionally dependent.
We examined these issues in a large sample of older adults that have been followed up for over 12 years. However, a few study limitations should be noted. Our sample consists of a genetically homogenous sample of Ashkenazi Jewish older adults; therefore, the results may not be generalizable to all community-dwelling older adults. Also, participants were well-educated and with low levels of comorbidities. This resulted in a lower prevalence of mobility disability compared to other community based studies (in community-dwelling older women the prevalence was ~30%) [29]. Our gait measures were based on a single walk over an 8.5-meter walkway (corresponding to a mean of 19 steps at baseline). This may have affected the reliability of gait measures (particularly variability), but in community-dwelling older adults ~16 steps are known to provide fair to good reliability for gait measures [30].
Conclusions
With advancing age, the pace domain (gait speed and step length) declined in an accelerating non-linear fashion whereas rhythm (step time) increased in an accelerating non-linear fashion. In contrast, variability increased in a gradual, linear fashion. The rates of change in pace and rhythm were further modified by cognitive impairment (pace and variability) and mobility disability (rhythm only).
Supplementary Material
Supplementary Figure 1. Changes in pace and rhythm in those with memory and non-memory related cognitive impairment at baseline
Highlights.
Pace, rhythm and variability represent unique gait domains
Pace declined in an accelerating non-linear fashion with increasing age
Rhythm (non-linearly) and variability (linearly) increased with age
Cognitive impairment was associated with faster changes in pace and rhythm
Mobility disability was associated with faster increases in rhythm
Acknowledgements:
We thank the study participants for their contribution
Funding resources
National Institutes of Health/National Institute on Aging (NIH/NIA) R01AG062659-01A1, NIH/NIA (PI: Helena Blumen), R01AG057548-01A1 (PI: Joe Verghese), R01AG061155-01 (PI: Sofiya Milman) and R01AG057909 (PI: Nir Barzilai)
Footnotes
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Conflict of Interest
J Verghese is on the advisory board of Catch-U, Inc, USA and MedRhythms, Inc., USA. Other authors declare no conflict of interest
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Supplementary Materials
Supplementary Figure 1. Changes in pace and rhythm in those with memory and non-memory related cognitive impairment at baseline