Structural brain signatures of frailty, defined as accumulation of self-reported health deficits in older adults

Raquel Gutiérrez-Zúñiga; James R.C. Davis; Kathy Ruddy; Céline De Looze; Daniel Carey; James Meaney; Rose Anne Kenny; Silvin Paul Knight; Roman Romero-Ortuno

doi:10.3389/fnagi.2023.1065191

Structural brain signatures of frailty, defined as accumulation of self-reported health deficits in older adults

Raquel Gutiérrez-Zúñiga^*, James R.C. Davis, Kathy Ruddy, Céline De Looze, Daniel Carey, James Meaney, Rose Anne Kenny, Silvin Paul Knight, Roman Romero-Ortuno

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

3 Citations (Scopus)

29 Downloads (Pure)

Abstract

Background: Frailty in older adults has been associated with reduced brain health. However, structural brain signatures of frailty remain understudied. Our aims were: (1) Explore associations between a frailty index (FI) and brain structure on magnetic resonance imaging (MRI). (2) Identify the most important FI features driving the associations.

Methods: We designed a cross-sectional observational study from a population-based study (The Irish Longitudinal Study on Aging: TILDA). Participants aged ≥50 years who underwent the wave 3 MRI sub-study were included. We measured cortex, basal ganglia, and each of the Desikan-Killiany regional volumes. Age-and sex-adjusted correlations were performed with a 32-item self-reported FI that included conditions commonly tested for frailty in research and clinical settings. A graph theory analysis of the network composed by each FI item and cortex volume was performed. White matter fiber integrity was quantified using diffusion tensor imaging (DTI).

Results: In 523 participants (mean age 69, 49% men), lower cortex and thalamic volumes were independently associated with higher FI. Sensory and functional difficulties, diabetes, polypharmacy, knee pain, and self-reported health were the main FI associations with cortex volume. In the network analysis, cortex volume had a modest influence within the frailty network. Regionally, higher FI was significantly associated with lower volumes in both orbitofrontal and temporal cortices. DTI analyses revealed inverse associations between the FI and the integrity of some association bundles.

Conclusion: The FI used had a recognizable but subtle structural brain signature in this sample. Only some FI deficits were directly associated with cortex volume, suggesting scope for developing FIs that include metrics more specifically related with brain health in future aging neuroscience studies.

Original language	English
Article number	1065191
Journal	Frontiers in aging neuroscience
Volume	15
DOIs	https://doi.org/10.3389/fnagi.2023.1065191
Publication status	Published - 19 Jan 2023
Externally published	Yes

Bibliographical note

Funding Information:
TILDA was funded by the Irish Department of Health, Atlantic Philanthropies, and Irish Life. RG-Z and RR-O were funded by the Global Brain Health Institute, Trinity College Dublin. RR-O was also funded by a grant from Science Foundation Ireland 18/FRL/6188.

Publisher Copyright:
Copyright © 2023 Gutiérrez-Zúñiga, Davis, Ruddy, De Looze, Carey, Meaney, Kenny, Knight and Romero-Ortuno.

Keywords

ageing
brain health
brain structure
frailty
magnetic resonance imaging

ASJC Scopus subject areas

Ageing
Cognitive Neuroscience

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Structural brain signatures of frailty, defined as accumulation of self-reported health deficits in older adults
Copyright 2023 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited.
Final published version, 4.54 MBLicence: CC BY

Cite this

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title = "Structural brain signatures of frailty, defined as accumulation of self-reported health deficits in older adults",

abstract = "Background: Frailty in older adults has been associated with reduced brain health. However, structural brain signatures of frailty remain understudied. Our aims were: (1) Explore associations between a frailty index (FI) and brain structure on magnetic resonance imaging (MRI). (2) Identify the most important FI features driving the associations.Methods: We designed a cross-sectional observational study from a population-based study (The Irish Longitudinal Study on Aging: TILDA). Participants aged ≥50 years who underwent the wave 3 MRI sub-study were included. We measured cortex, basal ganglia, and each of the Desikan-Killiany regional volumes. Age-and sex-adjusted correlations were performed with a 32-item self-reported FI that included conditions commonly tested for frailty in research and clinical settings. A graph theory analysis of the network composed by each FI item and cortex volume was performed. White matter fiber integrity was quantified using diffusion tensor imaging (DTI).Results: In 523 participants (mean age 69, 49% men), lower cortex and thalamic volumes were independently associated with higher FI. Sensory and functional difficulties, diabetes, polypharmacy, knee pain, and self-reported health were the main FI associations with cortex volume. In the network analysis, cortex volume had a modest influence within the frailty network. Regionally, higher FI was significantly associated with lower volumes in both orbitofrontal and temporal cortices. DTI analyses revealed inverse associations between the FI and the integrity of some association bundles.Conclusion: The FI used had a recognizable but subtle structural brain signature in this sample. Only some FI deficits were directly associated with cortex volume, suggesting scope for developing FIs that include metrics more specifically related with brain health in future aging neuroscience studies.",

keywords = "ageing, brain health, brain structure, frailty, magnetic resonance imaging",

author = "Raquel Guti{\'e}rrez-Z{\'u}{\~n}iga and Davis, {James R.C.} and Kathy Ruddy and {De Looze}, C{\'e}line and Daniel Carey and James Meaney and Kenny, {Rose Anne} and Knight, {Silvin Paul} and Roman Romero-Ortuno",

note = "Funding Information: TILDA was funded by the Irish Department of Health, Atlantic Philanthropies, and Irish Life. RG-Z and RR-O were funded by the Global Brain Health Institute, Trinity College Dublin. RR-O was also funded by a grant from Science Foundation Ireland 18/FRL/6188. Publisher Copyright: Copyright {\textcopyright} 2023 Guti{\'e}rrez-Z{\'u}{\~n}iga, Davis, Ruddy, De Looze, Carey, Meaney, Kenny, Knight and Romero-Ortuno.",

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T1 - Structural brain signatures of frailty, defined as accumulation of self-reported health deficits in older adults

AU - Gutiérrez-Zúñiga, Raquel

AU - Davis, James R.C.

AU - Ruddy, Kathy

AU - De Looze, Céline

AU - Carey, Daniel

AU - Meaney, James

AU - Kenny, Rose Anne

AU - Knight, Silvin Paul

AU - Romero-Ortuno, Roman

N1 - Funding Information: TILDA was funded by the Irish Department of Health, Atlantic Philanthropies, and Irish Life. RG-Z and RR-O were funded by the Global Brain Health Institute, Trinity College Dublin. RR-O was also funded by a grant from Science Foundation Ireland 18/FRL/6188. Publisher Copyright: Copyright © 2023 Gutiérrez-Zúñiga, Davis, Ruddy, De Looze, Carey, Meaney, Kenny, Knight and Romero-Ortuno.

PY - 2023/1/19

Y1 - 2023/1/19

N2 - Background: Frailty in older adults has been associated with reduced brain health. However, structural brain signatures of frailty remain understudied. Our aims were: (1) Explore associations between a frailty index (FI) and brain structure on magnetic resonance imaging (MRI). (2) Identify the most important FI features driving the associations.Methods: We designed a cross-sectional observational study from a population-based study (The Irish Longitudinal Study on Aging: TILDA). Participants aged ≥50 years who underwent the wave 3 MRI sub-study were included. We measured cortex, basal ganglia, and each of the Desikan-Killiany regional volumes. Age-and sex-adjusted correlations were performed with a 32-item self-reported FI that included conditions commonly tested for frailty in research and clinical settings. A graph theory analysis of the network composed by each FI item and cortex volume was performed. White matter fiber integrity was quantified using diffusion tensor imaging (DTI).Results: In 523 participants (mean age 69, 49% men), lower cortex and thalamic volumes were independently associated with higher FI. Sensory and functional difficulties, diabetes, polypharmacy, knee pain, and self-reported health were the main FI associations with cortex volume. In the network analysis, cortex volume had a modest influence within the frailty network. Regionally, higher FI was significantly associated with lower volumes in both orbitofrontal and temporal cortices. DTI analyses revealed inverse associations between the FI and the integrity of some association bundles.Conclusion: The FI used had a recognizable but subtle structural brain signature in this sample. Only some FI deficits were directly associated with cortex volume, suggesting scope for developing FIs that include metrics more specifically related with brain health in future aging neuroscience studies.

AB - Background: Frailty in older adults has been associated with reduced brain health. However, structural brain signatures of frailty remain understudied. Our aims were: (1) Explore associations between a frailty index (FI) and brain structure on magnetic resonance imaging (MRI). (2) Identify the most important FI features driving the associations.Methods: We designed a cross-sectional observational study from a population-based study (The Irish Longitudinal Study on Aging: TILDA). Participants aged ≥50 years who underwent the wave 3 MRI sub-study were included. We measured cortex, basal ganglia, and each of the Desikan-Killiany regional volumes. Age-and sex-adjusted correlations were performed with a 32-item self-reported FI that included conditions commonly tested for frailty in research and clinical settings. A graph theory analysis of the network composed by each FI item and cortex volume was performed. White matter fiber integrity was quantified using diffusion tensor imaging (DTI).Results: In 523 participants (mean age 69, 49% men), lower cortex and thalamic volumes were independently associated with higher FI. Sensory and functional difficulties, diabetes, polypharmacy, knee pain, and self-reported health were the main FI associations with cortex volume. In the network analysis, cortex volume had a modest influence within the frailty network. Regionally, higher FI was significantly associated with lower volumes in both orbitofrontal and temporal cortices. DTI analyses revealed inverse associations between the FI and the integrity of some association bundles.Conclusion: The FI used had a recognizable but subtle structural brain signature in this sample. Only some FI deficits were directly associated with cortex volume, suggesting scope for developing FIs that include metrics more specifically related with brain health in future aging neuroscience studies.

KW - ageing

KW - brain health

KW - brain structure

KW - frailty

KW - magnetic resonance imaging

U2 - 10.3389/fnagi.2023.1065191

DO - 10.3389/fnagi.2023.1065191

M3 - Article

AN - SCOPUS:85147305410

SN - 1663-4365

VL - 15

JO - Frontiers in aging neuroscience

JF - Frontiers in aging neuroscience

M1 - 1065191

ER -

Structural brain signatures of frailty, defined as accumulation of self-reported health deficits in older adults

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

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