Predicting brain age from functional connectivity in symptomatic and preclinical Alzheimer disease
“Brain-predicted age” quantifies apparent brain age compared to normative neuroimaging trajectories. Advanced brain-predicted age has been well established in symptomatic Alzheimer disease (AD), but is underexplored in preclinical AD. Prior brain-predicted age studies have typically used structural...
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-08-01
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| Series: | NeuroImage |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811922003524 |
| _version_ | 1811248514804482048 |
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| author | Peter R. Millar Patrick H. Luckett Brian A. Gordon Tammie L.S. Benzinger Suzanne E. Schindler Anne M. Fagan Carlos Cruchaga Randall J. Bateman Ricardo Allegri Mathias Jucker Jae-Hong Lee Hiroshi Mori Stephen P Salloway Igor Yakushev John C. Morris Beau M. Ances Sarah Adams, MS Ricardo Allegri, PhD Aki Araki Nicolas Barthelemy, PhD Randall Bateman, MD Jacob Bechara, BS Tammie Benzinger, MD, PhD Sarah Berman, MD, PhD Courtney Bodge, PhD Susan Brandon, BS William (Bill) Brooks, MBBS,MPH Jared Brosch, MD, PhD Jill Buck, BSN Virginia Buckles, PhD Kathleen Carter, PhD Lisa Cash, BFA Charlie Chen, BA Jasmeer Chhatwal, MD,PhD Patricio Chrem Mendez, MD Jasmin Chua, BS Helena Chui, MD Laura Courtney, BS Carlos Cruchaga, PhD Gregory S Day, MD Chrismary DeLaCruz, BA Darcy Denner, PhD Anna Diffenbacher, MS Aylin Dincer, BS Tamara Donahue, MS Jane Douglas, MPh Duc Duong, BS Noelia Egido, BS Bianca Esposito, BS Anne Fagan, PhD Marty Farlow, MD Becca Feldman, BS,BA Colleen Fitzpatrick, MS Shaney Flores, BS Nick Fox, MD Erin Franklin, MS Nelly Joseph-Mathurin, PhD Hisako Fujii, PhD Samantha Gardener, PhD Bernardino Ghetti, MD Alison Goate, PhD Sarah Goldberg, MS,LPC,NCC Jill Goldman, MS,MPhil,CGC Alyssa Gonzalez, BS Brian Gordon, PhD Susanne Gräber-Sultan, PhD Neill Graff-Radford, MD Morgan Graham, BA Julia Gray, MS Emily Gremminger, BA Miguel Grilo, MD Alex Groves Christian Haass, PhD Lisa Häsler, MSc Jason Hassenstab, PhD Cortaiga Hellm, BA Elizabeth Herries, BA Laura Hoechst-Swisher, MS Anna Hofmann, MD Anna Hofmann David Holtzman, MD Russ Hornbeck, MSCS, MPM Yakushev Igor, MD Ryoko Ihara, MD Takeshi Ikeuchi, MD Snezana Ikonomovic, MD Kenji Ishii, MD Clifford Jack, MD Gina Jerome, MS Erik Johnson, MD, PHD Mathias Jucker, PhD Celeste Karch, PhD Stephan Käser, PHD Kensaku Kasuga, MD Sarah Keefe, BS William Klunk, MD, PHD Robert Koeppe, PHD Deb Koudelis, MHS,RN Elke Kuder-Buletta, RN Christoph Laske, PhD Allan Levey, MD, PHD Johannes Levin, MD Yan Li, PHD Oscar Lopez, MD, MD Jacob Marsh, BA Ralph Martins, PhD Neal Scott Mason, PhD Colin Masters, MD Kwasi Mawuenyega, PhD Austin McCullough, PhD Candidate Eric McDade, DO Arlene Mejia, MD Estrella Morenas-Rodriguez, MD, PhD John Morris, MD James Mountz, MD Cath Mummery, PhD N eelesh Nadkarni, MD, PhD Akemi Nagamatsu, RN Katie Neimeyer, MS Yoshiki Niimi, MD James Noble, MD Joanne Norton, MSN, RN, PMHCNS-BC Brigitte Nuscher Ulricke Obermüller Antoinette O'Connor, MRCPI Riddhi Patira, MD Richard Perrin, MD, PhD Lingyan Ping, PhD Oliver Preische, MD Alan Renton, PhD John Ringman, MD Stephen Salloway, MD Peter Schofield, PhD Michio Senda, MD, PhD Nicholas T Seyfried, D.Phil Kristine Shady, BA, BS Hiroyuki Shimada, MD, PhD Wendy Sigurdson, RN Jennifer Smith, PhD Lori Smith, PA-C Beth Snitz, PhD Hamid Sohrabi, PhD Sochenda Stephens, BS, CCRP Kevin Taddei, BS Sarah Thompson, PA-C Jonathan Vöglein, MD Peter Wang, PhD Qing Wang, PhD Elise Weamer, MPH Chengjie Xiong, PhD Jinbin Xu, PhD Xiong Xu, BS, MS |
| author_facet | Peter R. Millar Patrick H. Luckett Brian A. Gordon Tammie L.S. Benzinger Suzanne E. Schindler Anne M. Fagan Carlos Cruchaga Randall J. Bateman Ricardo Allegri Mathias Jucker Jae-Hong Lee Hiroshi Mori Stephen P Salloway Igor Yakushev John C. Morris Beau M. Ances Sarah Adams, MS Ricardo Allegri, PhD Aki Araki Nicolas Barthelemy, PhD Randall Bateman, MD Jacob Bechara, BS Tammie Benzinger, MD, PhD Sarah Berman, MD, PhD Courtney Bodge, PhD Susan Brandon, BS William (Bill) Brooks, MBBS,MPH Jared Brosch, MD, PhD Jill Buck, BSN Virginia Buckles, PhD Kathleen Carter, PhD Lisa Cash, BFA Charlie Chen, BA Jasmeer Chhatwal, MD,PhD Patricio Chrem Mendez, MD Jasmin Chua, BS Helena Chui, MD Laura Courtney, BS Carlos Cruchaga, PhD Gregory S Day, MD Chrismary DeLaCruz, BA Darcy Denner, PhD Anna Diffenbacher, MS Aylin Dincer, BS Tamara Donahue, MS Jane Douglas, MPh Duc Duong, BS Noelia Egido, BS Bianca Esposito, BS Anne Fagan, PhD Marty Farlow, MD Becca Feldman, BS,BA Colleen Fitzpatrick, MS Shaney Flores, BS Nick Fox, MD Erin Franklin, MS Nelly Joseph-Mathurin, PhD Hisako Fujii, PhD Samantha Gardener, PhD Bernardino Ghetti, MD Alison Goate, PhD Sarah Goldberg, MS,LPC,NCC Jill Goldman, MS,MPhil,CGC Alyssa Gonzalez, BS Brian Gordon, PhD Susanne Gräber-Sultan, PhD Neill Graff-Radford, MD Morgan Graham, BA Julia Gray, MS Emily Gremminger, BA Miguel Grilo, MD Alex Groves Christian Haass, PhD Lisa Häsler, MSc Jason Hassenstab, PhD Cortaiga Hellm, BA Elizabeth Herries, BA Laura Hoechst-Swisher, MS Anna Hofmann, MD Anna Hofmann David Holtzman, MD Russ Hornbeck, MSCS, MPM Yakushev Igor, MD Ryoko Ihara, MD Takeshi Ikeuchi, MD Snezana Ikonomovic, MD Kenji Ishii, MD Clifford Jack, MD Gina Jerome, MS Erik Johnson, MD, PHD Mathias Jucker, PhD Celeste Karch, PhD Stephan Käser, PHD Kensaku Kasuga, MD Sarah Keefe, BS William Klunk, MD, PHD Robert Koeppe, PHD Deb Koudelis, MHS,RN Elke Kuder-Buletta, RN Christoph Laske, PhD Allan Levey, MD, PHD Johannes Levin, MD Yan Li, PHD Oscar Lopez, MD, MD Jacob Marsh, BA Ralph Martins, PhD Neal Scott Mason, PhD Colin Masters, MD Kwasi Mawuenyega, PhD Austin McCullough, PhD Candidate Eric McDade, DO Arlene Mejia, MD Estrella Morenas-Rodriguez, MD, PhD John Morris, MD James Mountz, MD Cath Mummery, PhD N eelesh Nadkarni, MD, PhD Akemi Nagamatsu, RN Katie Neimeyer, MS Yoshiki Niimi, MD James Noble, MD Joanne Norton, MSN, RN, PMHCNS-BC Brigitte Nuscher Ulricke Obermüller Antoinette O'Connor, MRCPI Riddhi Patira, MD Richard Perrin, MD, PhD Lingyan Ping, PhD Oliver Preische, MD Alan Renton, PhD John Ringman, MD Stephen Salloway, MD Peter Schofield, PhD Michio Senda, MD, PhD Nicholas T Seyfried, D.Phil Kristine Shady, BA, BS Hiroyuki Shimada, MD, PhD Wendy Sigurdson, RN Jennifer Smith, PhD Lori Smith, PA-C Beth Snitz, PhD Hamid Sohrabi, PhD Sochenda Stephens, BS, CCRP Kevin Taddei, BS Sarah Thompson, PA-C Jonathan Vöglein, MD Peter Wang, PhD Qing Wang, PhD Elise Weamer, MPH Chengjie Xiong, PhD Jinbin Xu, PhD Xiong Xu, BS, MS |
| author_sort | Peter R. Millar |
| collection | DOAJ |
| description | “Brain-predicted age” quantifies apparent brain age compared to normative neuroimaging trajectories. Advanced brain-predicted age has been well established in symptomatic Alzheimer disease (AD), but is underexplored in preclinical AD. Prior brain-predicted age studies have typically used structural MRI, but resting-state functional connectivity (FC) remains underexplored. Our model predicted age from FC in 391 cognitively normal, amyloid-negative controls (ages 18–89). We applied the trained model to 145 amyloid-negative, 151 preclinical AD, and 156 symptomatic AD participants to test group differences. The model accurately predicted age in the training set. FC-predicted brain age gaps (FC-BAG) were significantly older in symptomatic AD and significantly younger in preclinical AD compared to controls. There was minimal correspondence between networks predictive of age and AD. Elevated FC-BAG may reflect network disruption during symptomatic AD. Reduced FC-BAG in preclinical AD was opposite to the expected direction, and may reflect a biphasic response to preclinical AD pathology or may be driven by inconsistency between age-related vs. AD-related networks. Overall, FC-predicted brain age may be a sensitive AD biomarker. |
| first_indexed | 2024-04-12T15:29:27Z |
| format | Article |
| id | doaj.art-a5b21c8a2d4d47f7be6c84bca22f48e4 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-04-12T15:29:27Z |
| publishDate | 2022-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-a5b21c8a2d4d47f7be6c84bca22f48e42022-12-22T03:27:10ZengElsevierNeuroImage1095-95722022-08-01256119228Predicting brain age from functional connectivity in symptomatic and preclinical Alzheimer diseasePeter R. Millar0Patrick H. Luckett1Brian A. Gordon2Tammie L.S. Benzinger3Suzanne E. Schindler4Anne M. Fagan5Carlos Cruchaga6Randall J. Bateman7Ricardo Allegri8Mathias Jucker9Jae-Hong Lee10Hiroshi Mori11Stephen P Salloway12Igor Yakushev13John C. Morris14Beau M. Ances15Sarah Adams, MSRicardo Allegri, PhDAki ArakiNicolas Barthelemy, PhDRandall Bateman, MDJacob Bechara, BSTammie Benzinger, MD, PhDSarah Berman, MD, PhDCourtney Bodge, PhDSusan Brandon, BSWilliam (Bill) Brooks, MBBS,MPHJared Brosch, MD, PhDJill Buck, BSNVirginia Buckles, PhDKathleen Carter, PhDLisa Cash, BFACharlie Chen, BAJasmeer Chhatwal, MD,PhDPatricio Chrem Mendez, MDJasmin Chua, BSHelena Chui, MDLaura Courtney, BSCarlos Cruchaga, PhDGregory S Day, MDChrismary DeLaCruz, BADarcy Denner, PhDAnna Diffenbacher, MSAylin Dincer, BSTamara Donahue, MSJane Douglas, MPhDuc Duong, BSNoelia Egido, BSBianca Esposito, BSAnne Fagan, PhDMarty Farlow, MDBecca Feldman, BS,BAColleen Fitzpatrick, MSShaney Flores, BSNick Fox, MDErin Franklin, MSNelly Joseph-Mathurin, PhDHisako Fujii, PhDSamantha Gardener, PhDBernardino Ghetti, MDAlison Goate, PhDSarah Goldberg, MS,LPC,NCCJill Goldman, MS,MPhil,CGCAlyssa Gonzalez, BSBrian Gordon, PhDSusanne Gräber-Sultan, PhDNeill Graff-Radford, MDMorgan Graham, BAJulia Gray, MSEmily Gremminger, BAMiguel Grilo, MDAlex GrovesChristian Haass, PhDLisa Häsler, MScJason Hassenstab, PhDCortaiga Hellm, BAElizabeth Herries, BALaura Hoechst-Swisher, MSAnna Hofmann, MDAnna HofmannDavid Holtzman, MDRuss Hornbeck, MSCS, MPMYakushev Igor, MDRyoko Ihara, MDTakeshi Ikeuchi, MDSnezana Ikonomovic, MDKenji Ishii, MDClifford Jack, MDGina Jerome, MSErik Johnson, MD, PHDMathias Jucker, PhDCeleste Karch, PhDStephan Käser, PHDKensaku Kasuga, MDSarah Keefe, BSWilliam Klunk, MD, PHDRobert Koeppe, PHDDeb Koudelis, MHS,RNElke Kuder-Buletta, RNChristoph Laske, PhDAllan Levey, MD, PHDJohannes Levin, MDYan Li, PHDOscar Lopez, MD, MDJacob Marsh, BARalph Martins, PhDNeal Scott Mason, PhDColin Masters, MDKwasi Mawuenyega, PhDAustin McCullough, PhD CandidateEric McDade, DOArlene Mejia, MDEstrella Morenas-Rodriguez, MD, PhDJohn Morris, MDJames Mountz, MDCath Mummery, PhDN eelesh Nadkarni, MD, PhDAkemi Nagamatsu, RNKatie Neimeyer, MSYoshiki Niimi, MDJames Noble, MDJoanne Norton, MSN, RN, PMHCNS-BCBrigitte NuscherUlricke ObermüllerAntoinette O'Connor, MRCPIRiddhi Patira, MDRichard Perrin, MD, PhDLingyan Ping, PhDOliver Preische, MDAlan Renton, PhDJohn Ringman, MDStephen Salloway, MDPeter Schofield, PhDMichio Senda, MD, PhDNicholas T Seyfried, D.PhilKristine Shady, BA, BSHiroyuki Shimada, MD, PhDWendy Sigurdson, RNJennifer Smith, PhDLori Smith, PA-CBeth Snitz, PhDHamid Sohrabi, PhDSochenda Stephens, BS, CCRPKevin Taddei, BSSarah Thompson, PA-CJonathan Vöglein, MDPeter Wang, PhDQing Wang, PhDElise Weamer, MPHChengjie Xiong, PhDJinbin Xu, PhDXiong Xu, BS, MSDepartment of Neurology, Washington University, St. Louis, MO 63110, USA; Corresponding author.Department of Neurology, Washington University, St. Louis, MO 63110, USADepartment of Radiology, Washington University in St. Louis, St. Louis, MO, USADepartment of Radiology, Washington University in St. Louis, St. Louis, MO, USADepartment of Neurology, Washington University, St. Louis, MO 63110, USADepartment of Neurology, Washington University, St. Louis, MO 63110, USADepartment of Psychiatry, Washington University in St. Louis, St. Louis, MO, USADepartment of Neurology, Washington University, St. Louis, MO 63110, USADepartment of Cognitive Neurology, Institute for Neurological Research Fleni, Buenos Aires, ArgentinaGerman Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany; Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, GermanyDepartment of Neurology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, South KoreaDepartment of Clinical Neuroscience, Osaka City University Medical School, Nagaoka Sutoku University, Abenoku, Osaka 545-8585, JapanDepartment of Neurology, Brown University, Providence, RI, USADepartment of Nuclear Medicine, Technical University of Munich, Munich, GermanyDepartment of Neurology, Washington University, St. Louis, MO 63110, USADepartment of Neurology, Washington University, St. Louis, MO 63110, USA; Department of Radiology, Washington University in St. Louis, St. Louis, MO, USA“Brain-predicted age” quantifies apparent brain age compared to normative neuroimaging trajectories. Advanced brain-predicted age has been well established in symptomatic Alzheimer disease (AD), but is underexplored in preclinical AD. Prior brain-predicted age studies have typically used structural MRI, but resting-state functional connectivity (FC) remains underexplored. Our model predicted age from FC in 391 cognitively normal, amyloid-negative controls (ages 18–89). We applied the trained model to 145 amyloid-negative, 151 preclinical AD, and 156 symptomatic AD participants to test group differences. The model accurately predicted age in the training set. FC-predicted brain age gaps (FC-BAG) were significantly older in symptomatic AD and significantly younger in preclinical AD compared to controls. There was minimal correspondence between networks predictive of age and AD. Elevated FC-BAG may reflect network disruption during symptomatic AD. Reduced FC-BAG in preclinical AD was opposite to the expected direction, and may reflect a biphasic response to preclinical AD pathology or may be driven by inconsistency between age-related vs. AD-related networks. Overall, FC-predicted brain age may be a sensitive AD biomarker.http://www.sciencedirect.com/science/article/pii/S1053811922003524Brain agingAlzheimer diseaseResting-state functional connectivityfMRIMachine learning |
| spellingShingle | Peter R. Millar Patrick H. Luckett Brian A. Gordon Tammie L.S. Benzinger Suzanne E. Schindler Anne M. Fagan Carlos Cruchaga Randall J. Bateman Ricardo Allegri Mathias Jucker Jae-Hong Lee Hiroshi Mori Stephen P Salloway Igor Yakushev John C. Morris Beau M. Ances Sarah Adams, MS Ricardo Allegri, PhD Aki Araki Nicolas Barthelemy, PhD Randall Bateman, MD Jacob Bechara, BS Tammie Benzinger, MD, PhD Sarah Berman, MD, PhD Courtney Bodge, PhD Susan Brandon, BS William (Bill) Brooks, MBBS,MPH Jared Brosch, MD, PhD Jill Buck, BSN Virginia Buckles, PhD Kathleen Carter, PhD Lisa Cash, BFA Charlie Chen, BA Jasmeer Chhatwal, MD,PhD Patricio Chrem Mendez, MD Jasmin Chua, BS Helena Chui, MD Laura Courtney, BS Carlos Cruchaga, PhD Gregory S Day, MD Chrismary DeLaCruz, BA Darcy Denner, PhD Anna Diffenbacher, MS Aylin Dincer, BS Tamara Donahue, MS Jane Douglas, MPh Duc Duong, BS Noelia Egido, BS Bianca Esposito, BS Anne Fagan, PhD Marty Farlow, MD Becca Feldman, BS,BA Colleen Fitzpatrick, MS Shaney Flores, BS Nick Fox, MD Erin Franklin, MS Nelly Joseph-Mathurin, PhD Hisako Fujii, PhD Samantha Gardener, PhD Bernardino Ghetti, MD Alison Goate, PhD Sarah Goldberg, MS,LPC,NCC Jill Goldman, MS,MPhil,CGC Alyssa Gonzalez, BS Brian Gordon, PhD Susanne Gräber-Sultan, PhD Neill Graff-Radford, MD Morgan Graham, BA Julia Gray, MS Emily Gremminger, BA Miguel Grilo, MD Alex Groves Christian Haass, PhD Lisa Häsler, MSc Jason Hassenstab, PhD Cortaiga Hellm, BA Elizabeth Herries, BA Laura Hoechst-Swisher, MS Anna Hofmann, MD Anna Hofmann David Holtzman, MD Russ Hornbeck, MSCS, MPM Yakushev Igor, MD Ryoko Ihara, MD Takeshi Ikeuchi, MD Snezana Ikonomovic, MD Kenji Ishii, MD Clifford Jack, MD Gina Jerome, MS Erik Johnson, MD, PHD Mathias Jucker, PhD Celeste Karch, PhD Stephan Käser, PHD Kensaku Kasuga, MD Sarah Keefe, BS William Klunk, MD, PHD Robert Koeppe, PHD Deb Koudelis, MHS,RN Elke Kuder-Buletta, RN Christoph Laske, PhD Allan Levey, MD, PHD Johannes Levin, MD Yan Li, PHD Oscar Lopez, MD, MD Jacob Marsh, BA Ralph Martins, PhD Neal Scott Mason, PhD Colin Masters, MD Kwasi Mawuenyega, PhD Austin McCullough, PhD Candidate Eric McDade, DO Arlene Mejia, MD Estrella Morenas-Rodriguez, MD, PhD John Morris, MD James Mountz, MD Cath Mummery, PhD N eelesh Nadkarni, MD, PhD Akemi Nagamatsu, RN Katie Neimeyer, MS Yoshiki Niimi, MD James Noble, MD Joanne Norton, MSN, RN, PMHCNS-BC Brigitte Nuscher Ulricke Obermüller Antoinette O'Connor, MRCPI Riddhi Patira, MD Richard Perrin, MD, PhD Lingyan Ping, PhD Oliver Preische, MD Alan Renton, PhD John Ringman, MD Stephen Salloway, MD Peter Schofield, PhD Michio Senda, MD, PhD Nicholas T Seyfried, D.Phil Kristine Shady, BA, BS Hiroyuki Shimada, MD, PhD Wendy Sigurdson, RN Jennifer Smith, PhD Lori Smith, PA-C Beth Snitz, PhD Hamid Sohrabi, PhD Sochenda Stephens, BS, CCRP Kevin Taddei, BS Sarah Thompson, PA-C Jonathan Vöglein, MD Peter Wang, PhD Qing Wang, PhD Elise Weamer, MPH Chengjie Xiong, PhD Jinbin Xu, PhD Xiong Xu, BS, MS Predicting brain age from functional connectivity in symptomatic and preclinical Alzheimer disease NeuroImage Brain aging Alzheimer disease Resting-state functional connectivity fMRI Machine learning |
| title | Predicting brain age from functional connectivity in symptomatic and preclinical Alzheimer disease |
| title_full | Predicting brain age from functional connectivity in symptomatic and preclinical Alzheimer disease |
| title_fullStr | Predicting brain age from functional connectivity in symptomatic and preclinical Alzheimer disease |
| title_full_unstemmed | Predicting brain age from functional connectivity in symptomatic and preclinical Alzheimer disease |
| title_short | Predicting brain age from functional connectivity in symptomatic and preclinical Alzheimer disease |
| title_sort | predicting brain age from functional connectivity in symptomatic and preclinical alzheimer disease |
| topic | Brain aging Alzheimer disease Resting-state functional connectivity fMRI Machine learning |
| url | http://www.sciencedirect.com/science/article/pii/S1053811922003524 |
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