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Multimodal lifestyle engagement patterns support cognitive stability beyond neuropathological burden
Alzheimer's Research & Therapy volume 15, Article number: 221 (2023)
Abstract
Background
Modifiable lifestyle behaviors account for a large proportion of dementia risk. However, the combined contributions of multidomain lifestyle patterns to cognitive aging are poorly understood, as most studies have examined individual lifestyle behaviors in isolation and without neuropathological characterization. This study examined data-driven patterns of lifestyle behaviors across multiple domains among older adults and tested their associations with disease-specific neuropathological burden and cognitive decline.
Methods
Participants included 2059 older adults enrolled in the longitudinal Memory and Aging Project (MAP) at the Rush Alzheimer’s Disease Center; none of whom had dementia at baseline (73% no cognitive impairment (NCI), 27% mild cognitive impairment [MCI]). All participants completed cognitive testing annually. Lifestyle factors were measured during at least one visit and included (1) actigraphy-measured physical activity, as well as self-reported (2) sleep quality, (3) life space, (4) cognitive activities, (5) social activities, and (6) social network. A subset of participants (n = 791) had autopsy data for which burden of Alzheimer’s disease (AD), cerebrovascular disease (CVD), Lewy body disease, and hippocampal sclerosis/TDP-43 was measured. Latent profile analysis across all 2059 participants identified distinct subgroups (i.e., classes) of lifestyle patterns. Linear mixed-effects models examined relationships between lifestyle classes and global cognitive trajectories, with and without covarying for all neuropathologies. Classes were also compared on rates of incident MCI/dementia.
Results
Five classes were identified: Class 1Low Life Space (lowest lifestyle engagement), Class 2PA (high physical activity), Class 3Low Avg (low to average lifestyle engagement), Class 4Balanced (high average lifestyle engagement), and Class 5Social (large social network). Classes 4Balanced and 5Social had the lowest AD burden, and Class 2PA had the lowest CVD burden. Classes 2–5 had significantly less steep global cognitive decline compared to Class 1Low Life Space, with comparable effect sizes before and after covarying for neuropathological burden. Classes 4Balanced and 5Social exhibited the lowest rates of incident MCI/dementia.
Conclusions
Lifestyle behavior patterns among older adults account for differential rates of cognitive decline and clinical progression. Those with at least average engagement across all lifestyle domains exhibit greater cognitive stability after adjustment for neuropathology, highlighting the importance of engagement in multiple healthy lifestyle behaviors for later life cognitive health.
Introduction
The prevalence of dementia is precipitously rising, yet development of cognitive impairment with age is not inevitable. Converging lines of evidence suggest that over 40% of dementia cases are attributable to modifiable exposures and lifestyle factors [1]. Optimal engagement in later life behaviors such as physical activity, sleep, and cognitive and social activities has each been linked with reduced cognitive decline, even among older adults with autosomal dominant genetic risk for dementia. These data underscore a key need to develop primary prevention approaches for brain health. Yet, despite significant advancements in our understanding of individual dementia prevention techniques, lifestyle behaviors do not occur in isolation, and holistic understanding of lifestyle patterns for dementia prevention has lagged.
Indeed, the vast majority of studies have examined potential neuroprotective behaviors one at a time, despite the high level of interconnection across such lifestyle factors. Therefore, little is known about whether specific neuroprotective patterns of lifestyle behaviors exist [2,3,4]. Previous work from Carlson and colleagues [5] showed that participation in a variety of lifestyle behaviors is most associated with reduced risk of cognitive aging or the development of dementia. Similarly, data from the randomized controlled FINGER trial demonstrate that a multimodal approach to lifestyle optimization can support cognitive health over a 2-year period in older adults at risk for dementia [6]. These and other studies suggest that a deeper understanding of multimodal lifestyle patterns for dementia prevention is highly warranted. However, most studies in this area do not account for interrelationships among multiple lifestyle factors [7, 8] or binarize (yes/no) these variables [9, 10], which may not fully capture the natural spectrum of behavior. Examining a wide range of lifestyle factors in combination is both ecologically valid and may provide additional insights into patterns that most strongly relate to better brain and cognitive outcomes.
Another limitation of the existing literature examining lifestyle behaviors and brain health is the lack of contextual neuropathological information available. For instance, animal models and some emerging human data indicate that physical activity and sleep may directly contribute to pathological burden as well as impact one’s ability to engage in neuroprotective behaviors [11,12,13,14]. These data suggest that understanding the neuropathological milieu may be highly relevant when disentangling the effects of lifestyle on cognitive health. Notably, of the studies that have examined lifestyle factors and resistance to pathological change (e.g., Alzheimer’s disease pathology), few have incorporated multiple facets of lifestyle [10, 11]. Understanding how modifiable risk factors associate with risk of specific pathology development and incrementally relate to cognitive health beyond neuropathological burden (e.g., disease stage) is important to inform person- and disease-specific brain health recommendations.
To better understand the combined contribution of multiple, modifiable lifestyle patterns on neuropathology burden and cognitive aging, we leveraged multimodal lifestyle and longitudinal cognitive data from adults without baseline dementia enrolled in the Rush Memory and Aging Project (MAP) neuropathology cohort. Prior work in this cohort has reported independent relationships among individual lifestyle factors (e.g., cognitive activities, physical activity, social engagement), cognitive change, and individual neuropathologies (e.g., AD burden) [11, 15, 16]. Here, we extend that work. We employed latent profile analysis to empirically derive subgroups of participants with similar behavior patterns across different lifestyle domains, including physical activity, cognitive activity, social engagement, sleep, and environmental enrichment. We examined the relationship between lifestyle patterns and neuropathology burden as well as longitudinal cognitive trajectories and rates of incident CI. Systematic model comparisons determined whether lifestyle pattern effects on cognition were comparable to, and independent of, the relative effects of disease burden across multiple neuropathologies.
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