Abstract

There is well-documented evidence of brain network differences between individuals with Alzheimer’s disease (AD) and healthy controls (HC). To date, imaging studies investigating brain networks in these populations have typically been cross-sectional, and the reproducibility of such findings is somewhat unclear. In a novel study, we use the longitudinal ADNI data on the whole brain to jointly compute the brain network at baseline and one-year using a state of the art approach that pools information across both time points to yield distinct visit-specific networks for the AD and HC cohorts, resulting in more accurate inferences. We perform a multiscale comparison of the AD and HC networks in terms of global network metrics as well as at the more granular level of resting state networks defined under a whole brain parcellation. Our analysis illustrates a decrease in small-worldedness in the AD group at both the time points and also identifies more local network features and hub nodes that are disrupted due to the progression of AD. We also obtain high reproducibility of the HC network across visits. On the other hand, a separate estimation of the networks at each visit using standard graphical approaches reveals fewer meaningful differences and lower reproducibility.

Details

Title
A Novel Joint Brain Network Analysis Using Longitudinal Alzheimer’s Disease Data
Author
Kundu, Suprateek 1   VIAFID ORCID Logo  ; Lukemire, Joshua 1 ; Wang, Yikai 1 ; Guo, Ying 1 ; Weiner, Michael W 2 ; Schuff, Norbert 3 ; Rosen, Howard J 2 ; Miller, Bruce L 2 ; Neylan, Thomas 2 ; Hayes, Jacqueline 2 ; Finley, Shannon 2 ; Aisen, Paul 4 ; Khachaturian, Zaven 5 ; Thomas, Ronald G 4 ; Donohue, Michael 4 ; Walter, Sarah 4 ; Gessert, Devon 4 ; Sather, Tamie 4 ; Jiminez, Gus 4 ; Thal, Leon 4 ; Brewer, James 4 ; Vanderswag, Helen 4 ; Fleisher, Adam 4 ; Davis, Melissa 4 ; Morrison, Rosemary 4 ; Petersen, Ronald 6 ; Jack, Clifford R 6 ; Bernstein, Matthew 6 ; Borowski, Bret 6 ; Gunter, Jeff 6 ; Senjem, Matt 6 ; Vemuri, Prashanthi 6 ; Jones, David 6 ; Kantarci, Kejal 6 ; Ward, Chad 6 ; Mason, Sara S 6 ; Albers, Colleen S 6 ; Knopman, David 6 ; Johnson, Kris 6 ; Jagust, William 7 ; Landau, Susan 7 ; Trojanowki, John Q 8 ; Shaw, Leslie M 8 ; Lee, Virginia 8 ; Korecka, Magdalena 8 ; Figurski, Michal 8 ; Arnold, Steven E 8 ; Karlawish, Jason H 8 ; Wolk, David 8 ; Toga, Arthur W 9 ; Crawford, Karen 9 ; Neu, Scott 9 ; Schneider, Lon S 9 ; Pawluczyk, Sonia 9 ; Beccera, Mauricio 9 ; Liberty Teodoro 9 ; Spann, Bryan M 9 ; Beckett, Laurel 10 ; Harvey, Danielle 10 ; Fletcher, Evan 10 ; Carmichael, Owen 10 ; Olichney, John 10 ; DeCarli, Charles 10 ; Green, Robert C 11 ; Sperling, Reisa A 11 ; Johnson, Keith A 11 ; Marshall, Gad 11 ; Frey, Meghan 11 ; Lane, Barton 11 ; Rosen, Allyson 11 ; Tinklenberg, Jared 11 ; Saykin, Andrew J 12 ; Foroud, Tatiana M 12 ; Shen, Li 12 ; Faber, Kelley 12 ; Kim, Sungeun 12 ; Nho, Kwangsik 12 ; Farlow, Martin R 12 ; Hake, AnnMarie 12 ; Matthews, Brandy R 12 ; Herring, Scott 12 ; Hunt, Cynthia 12 ; Morris, John 13 ; Raichle, Marc 13 ; Holtzman, Davie 13 ; Cairns, Nigel J 13 ; Householder, Erin 13 ; Taylor-Reinwald, Lisa 13 ; Ances, Beau 13 ; Carroll, Maria 13 ; Leon, Sue 13 ; Mintun, Mark A 13 ; Schneider, Stacy 13 ; Oliver, Angela 13 ; Raudin, Lisa 14 ; Sorensen, Greg 15 ; Kuller, Lew 16 ; Mathis, Chet 16 ; Lopez, Oscar L 16 ; Oakley, MaryAnn 16 ; Paul, Steven 17 ; Relkin, Norman 17 ; Chaing, Gloria 17 ; Davies, Peter 18 ; Fillit, Howard 19 ; Hefti, Franz 20 ; Mesulam, M Marcel 21 ; Kerwin, Diana 21 ; Marek-Marsel Mesulam 21 ; Lipowski, Kristine 21 ; Chuang-Kuo, Wu 21 ; Johnson, Nancy 21 ; Grafman, Jordan 21 ; Potter, William 22 ; Snyder, Peter 23 ; Schwartz, Adam 24 ; Montine, Tom 25 ; Peskind, Elaine R 25 ; Fox, Nick 26 ; Thompson, Paul 27 ; Apostolova, Liana 27 ; Tingus, Kathleen 27 ; Woo, Ellen 27 ; Silverman, Daniel H S 27 ; Lu, Po H 27 ; Bartzokis, George 27 ; Koeppe, Robert A 28 ; Heidebrink, Judith L 28 ; Lord, Joanne L 28 ; Potkin, Steven G 28 ; Preda, Adrian 28 ; Nguyenv, Dana 28 ; Foster, Norm 29 ; Reiman, Eric M 30 ; Chen, Kewei 30 ; Tariot, Pierre 30 ; Reeder, Stephanie 30 ; Potkin, Steven 31 ; Mulnard, Ruth A 31 ; Thai, Gaby 31 ; Mc-Adams-Ortiz, Catherine 31 ; Buckholtz, Neil 32 ; Hsiao, John 32 ; Albert, Marylyn 33 ; Albert, Marilyn 33 ; Onyike, Chiadi 33 ; Daniel D’Agostino 33 ; Kielb, Stephanie 33 ; Simpson, Donna M 33 ; Frank, Richard 34 ; Kaye, Jeffrey 35 ; Quinn, Joseph 35 ; Lind, Betty 35 ; Carter, Raina 35 ; Dolen, Sara 35 ; Doody, Rachelle S 36 ; Villanueva-Meyer, Javier 36 ; Chowdhury, Munir 36 ; Rountree, Susan 36 ; Dang, Mimi 36 ; Stern, Yaakov 36 ; Honig, Lawrence S 36 ; Bell, Karen L 36 ; Marson, Daniel 37 ; Griffith, Randall 37 ; Clark, David 37 ; Geldmacher, David 37 ; Brockington, John 37 ; Roberson, Erik 37 ; Grossman, Hillel 38 ; Mitsis, Effie 38 ; Leyla de Toledo-Morrell 39 ; Shah, Raj C 39 ; Fleischman, Debra 39 ; Arfanakis, Konstantinos 39 ; Duara, Ranjan 40 ; Varon, Daniel 40 ; Greig, Maria T 40 ; Roberts, Peggy 40 ; Galvin, James E 41 ; Cerbone, Brittany 41 ; Michel, Christina A 41 ; Rusinek, Henry 41 ; de Leon, Mony J 41 ; Glodzik, Lidia 41 ; De Santi, Susan 41 ; Doraiswamy, P Murali 42 ; Petrella, Jeffrey R 42 ; Wong, Terence Z 42 ; James, Olga 42 ; Smith, Charles D 43 ; Jicha, Greg 43 ; Hardy, Peter 43 ; Sinha, Partha 43 ; Oates, Elizabeth 43 ; Conrad, Gary 43 ; Porsteinsson, Anton P 44 ; Goldstein, Bonnie S 44 ; Kim, Martin 44 ; Makino, Kelly M 44 ; M Saleem Ismail 44 ; Brand, Connie 44 ; Womack, Kyle 45 ; Mathews, Dana 45 ; Quiceno, Mary 45 ; Diaz-Arrastia, Ramon 45 ; King, Richard 45 ; Weiner, Myron 45 ; Martin-Cook, Kristen 45 ; DeVous, Michael 45 ; Levey, Allan I 46 ; Lah, James J 46 ; Cellar, Janet S 46 ; Burns, Jeffrey M 47 ; Anderson, Heather S 47 ; Swerdlow, Russell H 47 ; Graff-Radford, Neill R 48 ; Parfitt, Francine 48 ; Kendall, Tracy 48 ; Johnson, Heather 48 ; van Dyck, Christopher H 49 ; Carson, Richard E 49 ; MacAvoy, Martha G 49 ; Chertkow, Howard 50 ; Bergman, Howard 50 ; Hosein, Chris 50 ; Black, Sandra 51 ; Stefanovic, Bojana 51 ; Caldwell, Curtis 51 ; Hsiung, Ging-Yuek Robin 52 ; Feldman, Howard 52 ; Mudge, Benita 52 ; Assaly, Michele 52 ; Kertesz, Andrew 53 ; Rogers, John 53 ; Bernick, Charles 53 ; Munic, Donna 53 ; Finger, Elizabether 54 ; Pasternak, Stephen 54 ; Rachinsky, Irina 54 ; Drost, Dick 54 ; Sadowsky, Carl 55 ; Martinez, Walter 55 ; Villena, Teresa 55 ; Turner, Raymond Scott 56 ; Johnson, Kathleen 56 ; Reynolds, Brigid 56 ; Sabbagh, Marwan N 57 ; Belden, Christine M 57 ; Jacobson, Sandra A 57 ; Sirrel, Sherye A 57 ; Kowall, Neil 58 ; Killiany, Ronald 58 ; Budson, Andrew E 58 ; Norbash, Alexander 58 ; Johnson, Patricia Lynn 58 ; Allard, Joanne 59 ; Lerner, Alan 60 ; Ogrocki, Paula 60 ; Hudson, Leon 60 ; Kittur, Smita 61 ; Borrie, Michael 62 ; T-Y, Lee 62 ; Bartha, Rob 62 ; Johnson, Sterling 63 ; Asthana, Sanjay 63 ; Carlsson, Cynthia M 63 ; Fruehling, J Jay 63 ; Harding, Sandra 63 ; Bates, Vernice 64 ; Capote, Horacio 64 ; Rainka, Michelle 64 ; Scharre, Douglas W 65 ; Kataki, Maria 65 ; Adeli, Anahita 65 ; Petrie, Eric C 65 ; Li, Gail 65 ; Zimmerman, Earl A 66 ; Celmins, Dzintra 66 ; Brown, Alice D 66 ; Pearlson, Godfrey D 67 ; Blank, Karen 67 ; Anderson, Karen 67 ; Santulli, Robert B 68 ; Kitzmiller, Tamar J 68 ; Schwartz, Eben S 68 ; Sink, Kaycee M 69 ; Williamson, Jeff D 69 ; Garg, Pradeep 69 ; Watkins, Franklin 69 ; Ott, Brian R 70 ; Querfurth, Henry 70 ; Tremont, Geoffrey 70 ; Salloway, Stephen 71 ; Malloy, Paul 71 ; Correia, Stephen 71 ; Mintzer, Jacobo 72 ; Spicer, Kenneth 72 ; Bachman, David 72 ; Massoglia, Dino 72 ; Pomara, Nunzio 73 ; Hernando, Raymundo 73 ; Sarrael, Antero 73 ; Schultz, Susan K 74 ; Boles Ponto, Laura L 74 ; Shim, Hyungsub 74 ; Smith, Karen Elizabeth 74 ; Smith, Amanda 75 ; Fargher, Kristin 75 ; Balebail, Ashok Raj 75 ; Friedl, Karl 76 ; Yesavage, Jerome A 77 ; Taylor, Joy L 77 ; Furst, Ansgar J 77 

 Department of Biostatistics and Bioinformatics, Emory University, Atlanta, Ga, USA 
 UC San Francisco, California, USA 
 UC San Francisco, California, USA; UC Davis, California, USA 
 UC San Diego, California, USA 
 UC San Diego, California, USA; Prevent Alzheimer’s Disease, Rockville, Maryland, USA 
 Mayo Clinic, Rochester, New York, USA 
 UC Berkeley, California, USA 
 UPenn, Philadelphia, Pennsylvania, USA 
 USC, Los Angeles, California, USA 
10  UC Davis, California, USA 
11  Brigham and Women’s Hospital/Harvard Medical School, Boston, Massachusetts, USA 
12  Indiana University, Bloomington, Indiana, USA 
13  Washington University St Louis, Missouri, USA 
14  Prevent Alzheimer’s Disease, Rockville, Maryland, USA 
15  Siemens, Munich, Germany 
16  University of Pittsburg, Pennsylvania, USA 
17  Cornell University, Ithaca, New York, USA 
18  Albert Einstein College of Medicine of Yeshiva University, Bronx, New York, USA 
19  AD Drug Discovery Foundation, New York City, New York, USA 
20  Acumen Pharmaceuticals, Livermore, California, USA 
21  Northwestern University, Evanston and Chicago, Illinois, USA 
22  National Institute of Mental Health, Rockville, Maryland, USA 
23  Brown University, Providence, Rhode Island, USA 
24  Eli Lilly, Indianapolis, Indiana, USA 
25  University of Washington, Seattle, Washington, USA 
26  University of London, London, England 
27  UCLA, Los Angeles, California, USA 
28  University of Michigan, Ann Arbor, Michigan, USA 
29  University of Utah, Salt Lake, Utah, USA 
30  Banner Alzheimer’s Institute, Phoenix, Arizona, USA 
31  UC Irvine, Irvine, California, USA 
32  National Institute on Aging, Bethesda, Maryland, USA 
33  Johns Hopkins University, Baltimore, Maryland, USA 
34  Richard Frank Consulting, Washington, DC, USA 
35  Oregon Health and Science University, Portland, Oregon, USA 
36  Baylor College of Medicine, Houston, Texas, USA 
37  University of Alabama, Birmingham, Alabama, USA 
38  Mount Sinai School of Medicine, New York City, New York, USA 
39  Rush University Medical Center, Chicago, Illinois, USA 
40  Wien Center, Miami, Florida, USA 
41  New York University, New York City, New York, USA 
42  Duke University Medical Center, Durham, North Carolina, USA 
43  University of Kentucky, Lexington, Kentucky, USA 
44  University of Rochester Medical Center, Rochester, New York, USA 
45  University of Texas Southwestern Medical School, Dallas, Texas, USA 
46  Emory University, Atlanta, Georgia, USA 
47  University of Kansas, Medical Center, Kansas City, Kansas, USA 
48  Mayo Clinic, Jacksonville, Florida, USA 
49  Yale University School of Medicine, New Haven, Connecticut, USA 
50  McGill University/Montreal-Jewish General Hospital, Montreal, Quebec, Canada 
51  Sunnybrook Health Sciences, Toronto, Ontario, Canada 
52  U.B.C. Clinic for AD & Related Disorders, Vancouver, British Columbia, Canada 
53  Cognitive Neurology–St Joseph’s, London, Ontario, Canada 
54  St Joseph’s Health Care, London, Ontario, Canada 
55  Premiere Research Institute, Palm Beach Neurology, Miami, Florida, USA 
56  Georgetown University Medical Center, Washington, DC, USA 
57  Banner Sun Health Research Institute, Sun City, Arizona, USA 
58  Boston University, Boston, Massachusetts, USA 
59  Howard University, Washington, DC, USA 
60  Case Western Reserve University, Cleveland, Ohio, USA 
61  Neurological Care of CNY, Liverpool, New York, USA 
62  Parkwood Hospital, London, Ontario, USA 
63  University of Wisconsin, Madison, Wisconsin, USA 
64  Dent Neurologic Institute, Amherst, New York, USA 
65  Ohio State University, Columbus, Ohio, USA 
66  Albany Medical College, Albany, New York, USA 
67  Hartford Hospital, Olin Neuropsychiatry Research Center, Hartford, Connecticut, USA 
68  Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire, USA 
69  Wake Forest University Health Sciences, Winston-Salem, North Carolina, USA 
70  Rhode Island Hospital, Providence, Rhode Island, USA 
71  Butler Hospital, Providence, Rhode Island, USA 
72  Medical University South Carolina, Charleston, South Carolina, USA 
73  Nathan Kline Institute, Orangeburg, New York, USA 
74  University of Iowa College of Medicine, Iowa City, Iowa, USA 
75  University of South Florida: USF Health Byrd Alzheimer’s Institute, Tampa, Florida, USA 
76  Department of Defense, Arlington, Virginia, USA 
77  Stanford University, Stanford, California, USA 
Pages
1-18
Publication year
2019
Publication date
Dec 2019
Publisher
Nature Publishing Group
e-ISSN
20452322
Source type
Scholarly Journal
Language of publication
English
ProQuest document ID
2329326570
Copyright
© 2019. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.