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

for the ADNI

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

for the ADNI

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

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

Keywords

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

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10.1002/gps.5952

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@article{8602a82330fe46a289db28c638aa4d13,

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 = "{for the ADNI} and Adriana Cannizzaro and Lucas Ronat and {El Haffaf}, {Lyna Mariam} and Alexandru Hanganu and Michael Weiner and Paul Aisen and Michael Weiner 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 John Morris and Cairns, {Nigel J.} and Lisa Taylor-Reinwald and Trojanowki, {J. Q.} and Les Shaw and Lee, {Virginia M.Y.} and Magdalena Korecka and Toga, {Arthur W.} and Karen Crawford and Scott Neu and Saykin, {Andrew J.} and Foroud, {Tatiana M.} and Steven Potkin and Li Shen and Zaven Kachaturian and Richard Frank and Snyder, {Peter J.} and Susan Molchan and Jeffrey Kaye and Joseph Quinn and Betty Lind and Sara Dolen and Schneider, {Lon S.} and Sonia Pawluczyk and Spann, {Bryan M.} and James Brewer and Helen Vanderswag and Heidebrink, {Judith L.} and Lord, {Joanne L.} and Ronald Petersen and Kris Johnson and Doody, {Rachelle S.} and Javier Villanueva-Meyer and Munir Chowdhury and Yaakov Stern and Honig, {Lawrence S.} and Bell, {Karen L.} and Morris, {John C.} and Beau Ances and Maria Carroll and Sue Leon and Mintun, {Mark A.} and Stacy Schneider and Daniel Marson and Randall Griffith and David Clark and Hillel Grossman and Effie Mitsis and Aliza Romirowsky and Leyla deToledo-Morrell and Shah, {Raj C.} and Ranjan Duara and Daniel Varon and Peggy Roberts and Marilyn Albert and Chiadi Onyike and Stephanie Kielb and Henry Rusinek and {de Leon}, {Mony J.} and Lidia Glodzik and {De Santi}, Susan and Doraiswamy, {P. Murali} and Petrella, {Jeffrey R.} and Coleman, {R. Edward} and Arnold, {Steven E.} and Karlawish, {Jason H.} and David Wolk and Smith, {Charles D.} and Greg Jicha and Peter Hardy and Lopez, {Oscar L.} and Oakley, {Mary Ann} and Simpson, {Donna M.} and Porsteinsson, {Anton P.} and Goldstein, {Bonnie S.} and Kim Martin and Makino, {Kelly M.} and Ismail, {M. Saleem} and Connie Brand and Mulnard, {Ruth A.} and Gaby Thai and Catherine Mc-Adams-Ortiz and Kyle Womack and Dana Mathews and Mary Quiceno and Ramon Diaz-Arrastia and Richard King and Myron Weiner and Kristen Martin-Cook and Michael DeVous and Levey, {Allan I.} and Lah, {James J.} and Cellar, {Janet S.} and Burns, {Jeffrey M.} and Anderson, {Heather S.} and Swerdlow, {Russell H.} and Liana Apostolova and Lu, {Po H.} and George Bartzokis and Silverman, {Daniel H.S.} and Graff-Radford, {Neill R.} and Francine Parfitt and Heather Johnson and Farlow, {Martin R.} and Hake, {Ann Marie} and Matthews, {Brandy R.} and Scott Herring and {van Dyck}, {Christopher H.} and Carson, {Richard E.} and MacAvoy, {Martha G.} and Howard Chertkow and Howard Bergman and Chris Hosein and Sandra Black and Bojana Stefanovic and Curtis Caldwell and {Robin Hsiung}, {Ging Yuek} and Howard Feldman and Benita Mudge and Michele Assaly and Andrew Kertesz and John Rogers and Dick Trost and Charles Bernick and Donna Munic and Diana Kerwin and Mesulam, {Marek Marsel} and Kristina Lipowski and Wu, {Chuang Kuo} and Nancy Johnson and Carl Sadowsky and Walter Martinez and Teresa Villena and Turner, {Raymond Scott} and Kathleen Johnson and Brigid Reynolds and Sperling, {Reisa A.} and Johnson, {Keith A.} and Gad Marshall and Meghan Frey and Jerome Yesavage and Taylor, {Joy L.} and Barton Lane and Allyson Rosen and Jared Tinklenberg and Marwan Sabbagh and Christine Belden and Sandra Jacobson and Neil Kowall and Ronald Killiany and Budson, {Andrew E.}",

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

year = "2023",

month = jun,

doi = "10.1002/gps.5952",

language = "English",

volume = "38",

journal = "International Journal of Geriatric Psychiatry",

issn = "0885-6230",

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 - for the ADNI

AU - Cannizzaro, Adriana

AU - Ronat, Lucas

AU - El Haffaf, Lyna Mariam

AU - Hanganu, Alexandru

AU - Weiner, Michael

AU - Aisen, Paul

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 - Morris, John

AU - Cairns, Nigel J.

AU - Taylor-Reinwald, Lisa

AU - Trojanowki, J. Q.

AU - Shaw, Les

AU - Lee, Virginia M.Y.

AU - Korecka, Magdalena

AU - Toga, Arthur W.

AU - Crawford, Karen

AU - Neu, Scott

AU - Saykin, Andrew J.

AU - Foroud, Tatiana M.

AU - Potkin, Steven

AU - Shen, Li

AU - Kachaturian, Zaven

AU - Frank, Richard

AU - Snyder, Peter J.

AU - Molchan, Susan

AU - Kaye, Jeffrey

AU - Quinn, Joseph

AU - Lind, Betty

AU - Dolen, Sara

AU - Schneider, Lon S.

AU - Pawluczyk, Sonia

AU - Spann, Bryan M.

AU - Brewer, James

AU - Vanderswag, Helen

AU - Heidebrink, Judith L.

AU - Lord, Joanne L.

AU - Petersen, Ronald

AU - Johnson, Kris

AU - Doody, Rachelle S.

AU - Villanueva-Meyer, Javier

AU - Chowdhury, Munir

AU - Stern, Yaakov

AU - Honig, Lawrence S.

AU - Bell, Karen L.

AU - Morris, John C.

AU - Ances, Beau

AU - Carroll, Maria

AU - Leon, Sue

AU - Mintun, Mark A.

AU - Schneider, Stacy

AU - Marson, Daniel

AU - Griffith, Randall

AU - Clark, David

AU - Grossman, Hillel

AU - Mitsis, Effie

AU - Romirowsky, Aliza

AU - deToledo-Morrell, Leyla

AU - Shah, Raj C.

AU - Duara, Ranjan

AU - Varon, Daniel

AU - Roberts, Peggy

AU - Albert, Marilyn

AU - Onyike, Chiadi

AU - Kielb, Stephanie

AU - Rusinek, Henry

AU - de Leon, Mony J.

AU - Glodzik, Lidia

AU - De Santi, Susan

AU - Doraiswamy, P. Murali

AU - Petrella, Jeffrey R.

AU - Coleman, R. Edward

AU - Arnold, Steven E.

AU - Karlawish, Jason H.

AU - Wolk, David

AU - Smith, Charles D.

AU - Jicha, Greg

AU - Hardy, Peter

AU - Lopez, Oscar L.

AU - Oakley, Mary Ann

AU - Simpson, Donna M.

AU - Porsteinsson, Anton P.

AU - Goldstein, Bonnie S.

AU - Martin, Kim

AU - Makino, Kelly M.

AU - Ismail, M. Saleem

AU - Brand, Connie

AU - Mulnard, Ruth A.

AU - Thai, Gaby

AU - Mc-Adams-Ortiz, Catherine

AU - Womack, Kyle

AU - Mathews, Dana

AU - Quiceno, Mary

AU - Diaz-Arrastia, Ramon

AU - King, Richard

AU - Weiner, Myron

AU - Martin-Cook, Kristen

AU - DeVous, Michael

AU - Levey, Allan I.

AU - Lah, James J.

AU - Cellar, Janet S.

AU - Burns, Jeffrey M.

AU - Anderson, Heather S.

AU - Swerdlow, Russell H.

AU - Apostolova, Liana

AU - Lu, Po H.

AU - Bartzokis, George

AU - Silverman, Daniel H.S.

AU - Graff-Radford, Neill R.

AU - Parfitt, Francine

AU - Johnson, Heather

AU - Farlow, Martin R.

AU - Hake, Ann Marie

AU - Matthews, Brandy R.

AU - Herring, Scott

AU - van Dyck, Christopher H.

AU - Carson, Richard E.

AU - MacAvoy, Martha G.

AU - Chertkow, Howard

AU - Bergman, Howard

AU - Hosein, Chris

AU - Black, Sandra

AU - Stefanovic, Bojana

AU - Caldwell, Curtis

AU - Robin Hsiung, Ging Yuek

AU - Feldman, Howard

AU - Mudge, Benita

AU - Assaly, Michele

AU - Kertesz, Andrew

AU - Rogers, John

AU - Trost, Dick

AU - Bernick, Charles

AU - Munic, Donna

AU - Kerwin, Diana

AU - Mesulam, Marek Marsel

AU - Lipowski, Kristina

AU - Wu, Chuang Kuo

AU - Johnson, Nancy

AU - Sadowsky, Carl

AU - Martinez, Walter

AU - Villena, Teresa

AU - Turner, Raymond Scott

AU - Johnson, Kathleen

AU - Reynolds, Brigid

AU - Sperling, Reisa A.

AU - Johnson, Keith A.

AU - Marshall, Gad

AU - Frey, Meghan

AU - Yesavage, Jerome

AU - Taylor, Joy L.

AU - Lane, Barton

AU - Rosen, Allyson

AU - Tinklenberg, Jared

AU - Sabbagh, Marwan

AU - Belden, Christine

AU - Jacobson, Sandra

AU - Kowall, Neil

AU - Killiany, Ronald

AU - Budson, Andrew E.

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 - http://www.scopus.com/inward/record.url?scp=85162798838&partnerID=8YFLogxK

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

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