Associations between neuropsychiatric symptoms of affective and vegetative domains and brain morphology in aging people with mild cognitive impairment and Alzheimer's disease

doi:10.1002/gps.5952

Associations between neuropsychiatric symptoms of affective and vegetative domains and brain morphology in aging people with mild cognitive impairment and Alzheimer's disease

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

3 Scopus citations

Abstract

Objective: Neuropsychiatric symptoms (NPS) are common in mild cognitive impairment (MCI) and even more in Alzheimer's disease (AD). The symptom-based cluster including nighttime disturbances, depression, appetite changes, anxiety, and apathy (affective and vegetative symptoms) was associated with an increased risk of dementia in MCI and has common neuroanatomical associations. Our objective was to investigate the differences in brain morphology associations with affective and vegetative symptoms between three groups: cognitively normal older adults (CN), MCI and AD. Material and Methods: Alzheimer's Disease Neuroimaging Initiative data of 223 CN, 367 MCI and 175 AD, including cortical volumes, surface areas and thicknesses and severity scores of the five NPS were analyzed. A whole-brain vertex-wise general linear model was performed to test for intergroup differences (CN-MCI, CN-AD, AD-MCI) in brain morphology associations with five NPS. Multiple regressions were conducted to investigate cortical change as a function of NPS severity in the AD-MCI contrast. Results: We found (1) signature differences in nighttime disturbances associations with prefrontal regions in AD-MCI, (2) signature differences in NPS associations with temporal regions in AD-MCI for depression and in CN-AD for anxiety, (3) decreased temporal metrics in MCI as nighttime disturbances and depression severity increased, (4) decreased pars triangularis metrics in AD as nighttime disturbances and apathy severity increased. Conclusion: Each NPS seems to have a signature on brain morphology. Affective and vegetative NPS were primarily associated with prefrontal and temporal regions. These signatures open the possibility of potential future assessments of links between brain morphology and NPS on an individual level.

Original language	English
Article number	e5952
Journal	International Journal of Geriatric Psychiatry
Volume	38
Issue number	6
DOIs	https://doi.org/10.1002/gps.5952
State	Published - Jun 2023

Bibliographical note

Publisher Copyright:
© 2023 John Wiley & Sons Ltd.

Funding

This work was supported by a doctoral research scholarship Centre de recherche de l’Institut Universitaire de Gériatrie de Montréal (CRIUGM)—Volet B in collaboration with NiEmoLab and a Faculty of Medicine of the Université de Montréal merit scholarship given to Lucas Ronat, a doctoral research scholarship Centre de Recherche de l’Institut Universitaire de Gériatrie Montréal (CRIUGM)—Volet B in collaboration with NiEmoLab and a research bursary from NiEmoLab given to Lyna Mariam El Haffaf, as well as funding from the Parkinson Canada-Parkinson Quebec (2018-00355); IUGM Foundation; Fonds de Recherche du Québec Santé; Lemaire Foundation given to Alexandru Hanganu. Data collection and sharing for this project was funded by the Alzheimer's Disease Neuroimaging Initiative (ADNI) (National Institutes of Health Grant U01 AG024904) and DOD ADNI (Department of Defense award number W81XWH‐12‐2‐0012). ADNI is funded by the National Institute on Aging, the National Institute of Biomedical Imaging and Bioengineering, and through generous contributions from the following: AbbVie, Alzheimer's Association; Alzheimer's Drug Discovery Foundation; Araclon Biotech; BioClinica, Inc.; Biogen; Bristol‐Myers Squibb Company; CereSpir, Inc.; Cogstate; Eisai Inc.; Elan Pharmaceuticals, Inc.; Eli Lilly and Company; EuroImmun; F. Hoffmann‐La Roche Ltd and its affiliated company Genentech, Inc.; Fujirebio; GE Healthcare; IXICO Ltd.; Janssen Alzheimer Immunotherapy Research & Development, LLC.; Johnson & Johnson Pharmaceutical Research & Development LLC.; Lumosity; Lundbeck; Merck & Co., Inc.; Meso Scale Diagnostics, LLC.; NeuroRx Research; Neurotrack Technologies; Novartis Pharmaceuticals Corporation; Pfizer Inc.; Piramal Imaging; Servier; Takeda Pharmaceutical Company; and Transition Therapeutics. The Canadian Institutes of Health Research is providing funds to support ADNI clinical sites in Canada. Private sector contributions are facilitated by the Foundation for the National Institutes of Health ( www.fnih.org ). The grantee organization is the Northern California Institute for Research and Education, and the study is coordinated by the Alzheimer's Therapeutic Research Institute at the University of Southern California. ADNI data are disseminated by the Laboratory for NeuroImaging at the University of Southern California. This work was supported by a doctoral research scholarship Volet B in collaboration with NiEmoLab and a Faculty of Medicine of the Université de Montréal merit scholarship given to Lucas Ronat, a doctoral research scholarship Volet B in collaboration with NiEmoLab and a research bursary from NiEmoLab given to Lyna Mariam El Haffaf, as well as funding from the Parkinson Canada‐Parkinson Quebec (2018‐00355); IUGM Foundation; ; Lemaire Foundation given to Alexandru Hanganu. Centre de recherche de l’Institut Universitaire de Gériatrie de Montréal (CRIUGM)— Centre de Recherche de l’Institut Universitaire de Gériatrie Montréal (CRIUGM)— Fonds de Recherche du Québec Santé

Funders	Funder number
Araclon Biotech
Centre de recherche de l’Institut Universitaire de Gériatrie de Montréal
DOD ADNI
IUGM Foundation
Lemaire foundation
Parkinson Canada-Parkinson Quebec
Université de Montréal merit scholarship given	2018‐00355
National Institutes of Health (NIH)	U01 AG024904
U.S. Department of Defense	W81XWH‐12‐2‐0012
U.S. Department of Health & Human Services \| NIH \| National Institute on Aging (U.S. National Institute on Aging)
National Institute of Biomedical Imaging and Bioengineering
Alzheimer's Association
Alzheimer's Drug Discovery Foundation
Biogen IDEC
DoD Alzheimer's Disease Neuroimaging Initiative
BioClinica Inc.
AbbVie Canada
Fonds de Recherche du Québec-Santé

UN SDGs

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

SDG 3 Good Health and Well-being

Keywords

Alzheimer's disease
brain morphology
magnetic resonance imaging
mild cognitive impairment
neuroanatomy
neuropsychiatric symptoms

ASJC Scopus subject areas

Geriatrics and Gerontology
Psychiatry and Mental health

Access to Document

10.1002/gps.5952

Cite this

@article{ba6cdeca9dc744618c5561549fecc694,

title = "Associations between neuropsychiatric symptoms of affective and vegetative domains and brain morphology in aging people with mild cognitive impairment and Alzheimer's disease",

abstract = "Objective: Neuropsychiatric symptoms (NPS) are common in mild cognitive impairment (MCI) and even more in Alzheimer's disease (AD). The symptom-based cluster including nighttime disturbances, depression, appetite changes, anxiety, and apathy (affective and vegetative symptoms) was associated with an increased risk of dementia in MCI and has common neuroanatomical associations. Our objective was to investigate the differences in brain morphology associations with affective and vegetative symptoms between three groups: cognitively normal older adults (CN), MCI and AD. Material and Methods: Alzheimer's Disease Neuroimaging Initiative data of 223 CN, 367 MCI and 175 AD, including cortical volumes, surface areas and thicknesses and severity scores of the five NPS were analyzed. A whole-brain vertex-wise general linear model was performed to test for intergroup differences (CN-MCI, CN-AD, AD-MCI) in brain morphology associations with five NPS. Multiple regressions were conducted to investigate cortical change as a function of NPS severity in the AD-MCI contrast. Results: We found (1) signature differences in nighttime disturbances associations with prefrontal regions in AD-MCI, (2) signature differences in NPS associations with temporal regions in AD-MCI for depression and in CN-AD for anxiety, (3) decreased temporal metrics in MCI as nighttime disturbances and depression severity increased, (4) decreased pars triangularis metrics in AD as nighttime disturbances and apathy severity increased. Conclusion: Each NPS seems to have a signature on brain morphology. Affective and vegetative NPS were primarily associated with prefrontal and temporal regions. These signatures open the possibility of potential future assessments of links between brain morphology and NPS on an individual level.",

keywords = "Alzheimer's disease, brain morphology, magnetic resonance imaging, mild cognitive impairment, neuroanatomy, neuropsychiatric symptoms",

author = "Adriana Cannizzaro and Lucas Ronat and \{El Haffaf\}, \{Lyna Mariam\} and Alexandru Hanganu and Michael Weiner and Paul Aisen and Paul Aisen and Ronald Petersen and Jack, \{Clifford R.\} and William Jagust and Trojanowki, \{John Q.\} and Toga, \{Arthur W.\} and Laurel Beckett and Green, \{Robert C.\} and Saykin, \{Andrew J.\} and John Morris and Enchi Liu and Green, \{Robert C.\} and Tom Montine and Ronald Petersen and Paul Aisen and Anthony Gamst and Thomas, \{Ronald G.\} and Michael Donohue and Sarah Walter and Devon Gessert and Tamie Sather and Laurel Beckett and Danielle Harvey and Anthony Gamst and Michael Donohue and John Kornak and Jack, \{Clifford R.\} and Anders Dale and Matthew Bernstein and Joel Felmlee and Nick Fox and Paul Thompson and Norbert Schuff and Gene Alexander and Charles DeCarli and William Jagust and Dan Bandy and Koeppe, \{Robert A.\} and Norm Foster and Reiman, \{Eric M.\} and Kewei Chen and Chet Mathis and Greg Jicha and Richard King",

note = "Publisher Copyright: {\textcopyright} 2023 John Wiley \& Sons Ltd.",

year = "2023",

month = jun,

doi = "10.1002/gps.5952",

language = "English",

volume = "38",

number = "6",

}

TY - JOUR

T1 - Associations between neuropsychiatric symptoms of affective and vegetative domains and brain morphology in aging people with mild cognitive impairment and Alzheimer's disease

AU - Cannizzaro, Adriana

AU - Ronat, Lucas

AU - El Haffaf, Lyna Mariam

AU - Hanganu, Alexandru

AU - Weiner, Michael

AU - Aisen, Paul

AU - Petersen, Ronald

AU - Jack, Clifford R.

AU - Jagust, William

AU - Trojanowki, John Q.

AU - Toga, Arthur W.

AU - Beckett, Laurel

AU - Green, Robert C.

AU - Saykin, Andrew J.

AU - Morris, John

AU - Liu, Enchi

AU - Green, Robert C.

AU - Montine, Tom

AU - Petersen, Ronald

AU - Aisen, Paul

AU - Gamst, Anthony

AU - Thomas, Ronald G.

AU - Donohue, Michael

AU - Walter, Sarah

AU - Gessert, Devon

AU - Sather, Tamie

AU - Beckett, Laurel

AU - Harvey, Danielle

AU - Gamst, Anthony

AU - Donohue, Michael

AU - Kornak, John

AU - Jack, Clifford R.

AU - Dale, Anders

AU - Bernstein, Matthew

AU - Felmlee, Joel

AU - Fox, Nick

AU - Thompson, Paul

AU - Schuff, Norbert

AU - Alexander, Gene

AU - DeCarli, Charles

AU - Jagust, William

AU - Bandy, Dan

AU - Koeppe, Robert A.

AU - Foster, Norm

AU - Reiman, Eric M.

AU - Chen, Kewei

AU - Mathis, Chet

AU - Jicha, Greg

AU - King, Richard

PY - 2023/6

Y1 - 2023/6

N2 - Objective: Neuropsychiatric symptoms (NPS) are common in mild cognitive impairment (MCI) and even more in Alzheimer's disease (AD). The symptom-based cluster including nighttime disturbances, depression, appetite changes, anxiety, and apathy (affective and vegetative symptoms) was associated with an increased risk of dementia in MCI and has common neuroanatomical associations. Our objective was to investigate the differences in brain morphology associations with affective and vegetative symptoms between three groups: cognitively normal older adults (CN), MCI and AD. Material and Methods: Alzheimer's Disease Neuroimaging Initiative data of 223 CN, 367 MCI and 175 AD, including cortical volumes, surface areas and thicknesses and severity scores of the five NPS were analyzed. A whole-brain vertex-wise general linear model was performed to test for intergroup differences (CN-MCI, CN-AD, AD-MCI) in brain morphology associations with five NPS. Multiple regressions were conducted to investigate cortical change as a function of NPS severity in the AD-MCI contrast. Results: We found (1) signature differences in nighttime disturbances associations with prefrontal regions in AD-MCI, (2) signature differences in NPS associations with temporal regions in AD-MCI for depression and in CN-AD for anxiety, (3) decreased temporal metrics in MCI as nighttime disturbances and depression severity increased, (4) decreased pars triangularis metrics in AD as nighttime disturbances and apathy severity increased. Conclusion: Each NPS seems to have a signature on brain morphology. Affective and vegetative NPS were primarily associated with prefrontal and temporal regions. These signatures open the possibility of potential future assessments of links between brain morphology and NPS on an individual level.

AB - Objective: Neuropsychiatric symptoms (NPS) are common in mild cognitive impairment (MCI) and even more in Alzheimer's disease (AD). The symptom-based cluster including nighttime disturbances, depression, appetite changes, anxiety, and apathy (affective and vegetative symptoms) was associated with an increased risk of dementia in MCI and has common neuroanatomical associations. Our objective was to investigate the differences in brain morphology associations with affective and vegetative symptoms between three groups: cognitively normal older adults (CN), MCI and AD. Material and Methods: Alzheimer's Disease Neuroimaging Initiative data of 223 CN, 367 MCI and 175 AD, including cortical volumes, surface areas and thicknesses and severity scores of the five NPS were analyzed. A whole-brain vertex-wise general linear model was performed to test for intergroup differences (CN-MCI, CN-AD, AD-MCI) in brain morphology associations with five NPS. Multiple regressions were conducted to investigate cortical change as a function of NPS severity in the AD-MCI contrast. Results: We found (1) signature differences in nighttime disturbances associations with prefrontal regions in AD-MCI, (2) signature differences in NPS associations with temporal regions in AD-MCI for depression and in CN-AD for anxiety, (3) decreased temporal metrics in MCI as nighttime disturbances and depression severity increased, (4) decreased pars triangularis metrics in AD as nighttime disturbances and apathy severity increased. Conclusion: Each NPS seems to have a signature on brain morphology. Affective and vegetative NPS were primarily associated with prefrontal and temporal regions. These signatures open the possibility of potential future assessments of links between brain morphology and NPS on an individual level.

KW - Alzheimer's disease

KW - brain morphology

KW - magnetic resonance imaging

KW - mild cognitive impairment

KW - neuroanatomy

KW - neuropsychiatric symptoms

UR - https://www.scopus.com/pages/publications/85162798838

UR - https://www.scopus.com/pages/publications/85162798838#tab=citedBy

U2 - 10.1002/gps.5952

DO - 10.1002/gps.5952

M3 - Article

C2 - 37351584

AN - SCOPUS:85162798838

SN - 0885-6230

VL - 38

JO - International Journal of Geriatric Psychiatry

JF - International Journal of Geriatric Psychiatry

IS - 6

M1 - e5952

ER -

Associations between neuropsychiatric symptoms of affective and vegetative domains and brain morphology in aging people with mild cognitive impairment and Alzheimer's disease

Abstract

Bibliographical note

Funding

UN SDGs

Keywords

ASJC Scopus subject areas

Access to Document

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