Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy

doi:10.1212/WNL.0000000000002570

. 2016 Apr 12;86(15):1368-1376.

doi: 10.1212/WNL.0000000000002570. Epub 2016 Mar 16.

Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy

Erin E Sundermann¹, Anat Biegon², Leah H Rubin², Richard B Lipton², Wenzhu Mowrey², Susan Landau², Pauline M Maki²; Alzheimer's Disease Neuroimaging Initiative

Collaborators, Affiliations

Collaborators

Alzheimer's Disease Neuroimaging Initiative:
Michael Weiner, Paul Aisen, Michael Weiner, Paul Aisen, Ronald Petersen, Clifford R Jack Jr, William Jagust, John Q Trojanowki, Arthur W Toga, Laurel Beckett, Robert C Green, Andrew J Saykin, John Morris, Enchi Liu, Robert C Green, Tom Montine, Ronald Petersen, Paul Aisen, Anthony Gamst, Ronald G Thomas, Michael Donohue, Sarah Walter, Devon Gessert, Tamie Sather, Laurel Beckett, Danielle Harvey, Anthony Gamst, Michael Donohue, John Kornak, Clifford R Jack Jr, Anders Dale, Matthew Bernstein, Joel Felmlee, Nick Fox, Paul Thompson, Norbert Schuff, Gene Alexander, Charles DeCarli, William Jagust, Dan Bandy, Robert A Koeppe, Norm Foster, Eric M Reiman, Kewei Chen, Chet Mathis, John Morris, Nigel J Cairns, Lisa Taylor-Reinwald, J Q Trojanowki, Les Shaw, Virginia M Y Lee, Magdalena Korecka, Arthur W Toga, Karen Crawford, Scott Neu, Andrew J Saykin, Tatiana M Foroud, Steven Potkin, Li Shen, Zaven Kachaturian, Richard Frank, Peter J Snyder, Susan Molchan, Jeffrey Kaye, Joseph Quinn, Betty Lind, Sara Dolen, Lon S Schneider, Sonia Pawluczyk, Bryan M Spann, James Brewer, Helen Vanderswag, Judith L Heidebrink, Joanne L Lord, Ronald Petersen, Kris Johnson, Rachelle S Doody, Javier Villanueva-Meyer, Munir Chowdhury, Yaakov Stern, Lawrence S Honig, Karen L Bell, John C Morris, Beau Ances, Maria Carroll, Sue Leon, Mark A Mintun, Stacy Schneider, Daniel Marson, Randall Griffith, David Clark, Hillel Grossman, Effie Mitsis, Aliza Romirowsky, Leyla deToledo-Morrell, Raj C Shah, Ranjan Duara, Daniel Varon, Peggy Roberts, Marilyn Albert, Chiadi Onyike, Stephanie Kielb, Henry Rusinek, Mony J de Leon, Lidia Glodzik, Susan De Santi, P Murali Doraiswamy, Jeffrey R Petrella, R Edward Coleman, Steven E Arnold, Jason H Karlawish, David Wolk, Charles D Smith, Greg Jicha, Peter Hardy, Oscar L Lopez, MaryAnn Oakley, Donna M Simpson, Anton P Porsteinsson, Bonnie S Goldstein, Kim Martin, Kelly M Makino, M Saleem Ismail, Connie Brand, Ruth A Mulnard, Gaby Thai, Catherine Mc-Adams-Ortiz, Kyle Womack, Dana Mathews, Mary Quiceno, Ramon Diaz-Arrastia, Richard King, Myron Weiner, Kristen Martin-Cook, Michael DeVous, Allan I Levey, James J Lah, Janet S Cellar, Jeffrey M Burns, Heather S Anderson, Russell H Swerdlow, Liana Apostolova, Po H Lu, George Bartzokis, Daniel H S Silverman, Neill R Graff-Radford, Francine Parfitt, Heather Johnson, Martin R Farlow, Ann Marie Hake, Brandy R Matthews, Scott Herring, Christopher H van Dyck, Richard E Carson, Martha G MacAvoy, Howard Chertkow, Howard Bergman, Chris Hosein, Sandra Black, Bojana Stefanovic, Curtis Caldwell, Ging-Yuek Robin Hsiung, Howard Feldman, Benita Mudge, Michele Assaly, Andrew Kertesz, John Rogers, Dick Trost, Charles Bernick, Donna Munic, Diana Kerwin, Marek-Marsel Mesulam, Kristina Lipowski, Chuang-Kuo Wu, Nancy Johnson, Carl Sadowsky, Walter Martinez, Teresa Villena, Raymond Scott Turner, Kathleen Johnson, Brigid Reynolds, Reisa A Sperling, Keith A Johnson, Gad Marshall, Meghan Frey, Jerome Yesavage, Joy L Taylor, Barton Lane, Allyson Rosen, Jared Tinklenberg, Marwan Sabbagh, Christine Belden, Sandra Jacobson, Neil Kowall, Ronald Killiany, Andrew E Budson, Alexander Norbash, Patricia Lynn Johnson, Thomas O Obisesan, Saba Wolday, Salome K Bwayo, Alan Lerner, Leon Hudson, Paula Ogrocki, Evan Fletcher, Owen Carmichael, John Olichney, Charles DeCarli, Smita Kittur, Michael Borrie, T-Y Lee, Rob Bartha, Sterling Johnson, Sanjay Asthana, Cynthia M Carlsson, Steven G Potkin, Adrian Preda, Dana Nguyen, Pierre Tariot, Adam Fleisher, Stephanie Reeder, Vernice Bates, Horacio Capote, Michelle Rainka, Douglas W Scharre, Maria Kataki, Earl A Zimmerman, Dzintra Celmins, Alice D Brown, Godfrey D Pearlson, Karen Blank, Karen Anderson, Andrew J Saykin, Robert B Santulli, Eben S Schwartz, Kaycee M Sink, Jeff D Williamson, Pradeep Garg, Franklin Watkins, Brian R Ott, Henry Querfurth, Geoffrey Tremont, Stephen Salloway, Paul Malloy, Stephen Correia, Howard J Rosen, Bruce L Miller, Jacobo Mintzer, Crystal Flynn Longmire, Kenneth Spicer, Elizabether Finger, Irina Rachinsky, John Rogers, Andrew Kertesz, Dick Drost, Nunzio Pomara, Raymundo Hernando, Antero Sarrael, Susan K Schultz, Laura L Boles Ponto, Hyungsub Shim, Karen Elizabeth Smith, Norman Relkin, Gloria Chaing, Lisa Raudin, Amanda Smith, Kristin Fargher, Balebail Ashok Raj

Affiliations

¹ From the Einstein Aging Study and the Department of Neurology (E.E.S., R.B.L.) and the Department of Epidemiology and Population Health (W.M.), Albert Einstein College of Medicine, Bronx; Department of Neurology (A.B.), State University of New York, Stony Brook; Department of Psychiatry (L.H.R., P.M.M.), University of Illinois at Chicago; and Helen Wills Neuroscience Institute (S.L.), University of California, Berkeley. erin.sundermann@einstein.yu.edu.
² From the Einstein Aging Study and the Department of Neurology (E.E.S., R.B.L.) and the Department of Epidemiology and Population Health (W.M.), Albert Einstein College of Medicine, Bronx; Department of Neurology (A.B.), State University of New York, Stony Brook; Department of Psychiatry (L.H.R., P.M.M.), University of Illinois at Chicago; and Helen Wills Neuroscience Institute (S.L.), University of California, Berkeley.

PMID: 26984945
PMCID: PMC4831033
DOI: 10.1212/WNL.0000000000002570

Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy

Erin E Sundermann et al. Neurology. 2016.

. 2016 Apr 12;86(15):1368-1376.

doi: 10.1212/WNL.0000000000002570. Epub 2016 Mar 16.

Authors

Erin E Sundermann¹, Anat Biegon², Leah H Rubin², Richard B Lipton², Wenzhu Mowrey², Susan Landau², Pauline M Maki²; Alzheimer's Disease Neuroimaging Initiative

Collaborators

Alzheimer's Disease Neuroimaging Initiative:
Michael Weiner, Paul Aisen, Michael Weiner, Paul Aisen, Ronald Petersen, Clifford R Jack Jr, William Jagust, John Q Trojanowki, Arthur W Toga, Laurel Beckett, Robert C Green, Andrew J Saykin, John Morris, Enchi Liu, Robert C Green, Tom Montine, Ronald Petersen, Paul Aisen, Anthony Gamst, Ronald G Thomas, Michael Donohue, Sarah Walter, Devon Gessert, Tamie Sather, Laurel Beckett, Danielle Harvey, Anthony Gamst, Michael Donohue, John Kornak, Clifford R Jack Jr, Anders Dale, Matthew Bernstein, Joel Felmlee, Nick Fox, Paul Thompson, Norbert Schuff, Gene Alexander, Charles DeCarli, William Jagust, Dan Bandy, Robert A Koeppe, Norm Foster, Eric M Reiman, Kewei Chen, Chet Mathis, John Morris, Nigel J Cairns, Lisa Taylor-Reinwald, J Q Trojanowki, Les Shaw, Virginia M Y Lee, Magdalena Korecka, Arthur W Toga, Karen Crawford, Scott Neu, Andrew J Saykin, Tatiana M Foroud, Steven Potkin, Li Shen, Zaven Kachaturian, Richard Frank, Peter J Snyder, Susan Molchan, Jeffrey Kaye, Joseph Quinn, Betty Lind, Sara Dolen, Lon S Schneider, Sonia Pawluczyk, Bryan M Spann, James Brewer, Helen Vanderswag, Judith L Heidebrink, Joanne L Lord, Ronald Petersen, Kris Johnson, Rachelle S Doody, Javier Villanueva-Meyer, Munir Chowdhury, Yaakov Stern, Lawrence S Honig, Karen L Bell, John C Morris, Beau Ances, Maria Carroll, Sue Leon, Mark A Mintun, Stacy Schneider, Daniel Marson, Randall Griffith, David Clark, Hillel Grossman, Effie Mitsis, Aliza Romirowsky, Leyla deToledo-Morrell, Raj C Shah, Ranjan Duara, Daniel Varon, Peggy Roberts, Marilyn Albert, Chiadi Onyike, Stephanie Kielb, Henry Rusinek, Mony J de Leon, Lidia Glodzik, Susan De Santi, P Murali Doraiswamy, Jeffrey R Petrella, R Edward Coleman, Steven E Arnold, Jason H Karlawish, David Wolk, Charles D Smith, Greg Jicha, Peter Hardy, Oscar L Lopez, MaryAnn Oakley, Donna M Simpson, Anton P Porsteinsson, Bonnie S Goldstein, Kim Martin, Kelly M Makino, M Saleem Ismail, Connie Brand, Ruth A Mulnard, Gaby Thai, Catherine Mc-Adams-Ortiz, Kyle Womack, Dana Mathews, Mary Quiceno, Ramon Diaz-Arrastia, Richard King, Myron Weiner, Kristen Martin-Cook, Michael DeVous, Allan I Levey, James J Lah, Janet S Cellar, Jeffrey M Burns, Heather S Anderson, Russell H Swerdlow, Liana Apostolova, Po H Lu, George Bartzokis, Daniel H S Silverman, Neill R Graff-Radford, Francine Parfitt, Heather Johnson, Martin R Farlow, Ann Marie Hake, Brandy R Matthews, Scott Herring, Christopher H van Dyck, Richard E Carson, Martha G MacAvoy, Howard Chertkow, Howard Bergman, Chris Hosein, Sandra Black, Bojana Stefanovic, Curtis Caldwell, Ging-Yuek Robin Hsiung, Howard Feldman, Benita Mudge, Michele Assaly, Andrew Kertesz, John Rogers, Dick Trost, Charles Bernick, Donna Munic, Diana Kerwin, Marek-Marsel Mesulam, Kristina Lipowski, Chuang-Kuo Wu, Nancy Johnson, Carl Sadowsky, Walter Martinez, Teresa Villena, Raymond Scott Turner, Kathleen Johnson, Brigid Reynolds, Reisa A Sperling, Keith A Johnson, Gad Marshall, Meghan Frey, Jerome Yesavage, Joy L Taylor, Barton Lane, Allyson Rosen, Jared Tinklenberg, Marwan Sabbagh, Christine Belden, Sandra Jacobson, Neil Kowall, Ronald Killiany, Andrew E Budson, Alexander Norbash, Patricia Lynn Johnson, Thomas O Obisesan, Saba Wolday, Salome K Bwayo, Alan Lerner, Leon Hudson, Paula Ogrocki, Evan Fletcher, Owen Carmichael, John Olichney, Charles DeCarli, Smita Kittur, Michael Borrie, T-Y Lee, Rob Bartha, Sterling Johnson, Sanjay Asthana, Cynthia M Carlsson, Steven G Potkin, Adrian Preda, Dana Nguyen, Pierre Tariot, Adam Fleisher, Stephanie Reeder, Vernice Bates, Horacio Capote, Michelle Rainka, Douglas W Scharre, Maria Kataki, Earl A Zimmerman, Dzintra Celmins, Alice D Brown, Godfrey D Pearlson, Karen Blank, Karen Anderson, Andrew J Saykin, Robert B Santulli, Eben S Schwartz, Kaycee M Sink, Jeff D Williamson, Pradeep Garg, Franklin Watkins, Brian R Ott, Henry Querfurth, Geoffrey Tremont, Stephen Salloway, Paul Malloy, Stephen Correia, Howard J Rosen, Bruce L Miller, Jacobo Mintzer, Crystal Flynn Longmire, Kenneth Spicer, Elizabether Finger, Irina Rachinsky, John Rogers, Andrew Kertesz, Dick Drost, Nunzio Pomara, Raymundo Hernando, Antero Sarrael, Susan K Schultz, Laura L Boles Ponto, Hyungsub Shim, Karen Elizabeth Smith, Norman Relkin, Gloria Chaing, Lisa Raudin, Amanda Smith, Kristin Fargher, Balebail Ashok Raj

Affiliations

¹ From the Einstein Aging Study and the Department of Neurology (E.E.S., R.B.L.) and the Department of Epidemiology and Population Health (W.M.), Albert Einstein College of Medicine, Bronx; Department of Neurology (A.B.), State University of New York, Stony Brook; Department of Psychiatry (L.H.R., P.M.M.), University of Illinois at Chicago; and Helen Wills Neuroscience Institute (S.L.), University of California, Berkeley. erin.sundermann@einstein.yu.edu.
² From the Einstein Aging Study and the Department of Neurology (E.E.S., R.B.L.) and the Department of Epidemiology and Population Health (W.M.), Albert Einstein College of Medicine, Bronx; Department of Neurology (A.B.), State University of New York, Stony Brook; Department of Psychiatry (L.H.R., P.M.M.), University of Illinois at Chicago; and Helen Wills Neuroscience Institute (S.L.), University of California, Berkeley.

PMID: 26984945
PMCID: PMC4831033
DOI: 10.1212/WNL.0000000000002570

Abstract

Objective: To examine sex differences in the relationship between clinical symptoms related to Alzheimer disease (AD) (verbal memory deficits) and neurodegeneration (hippocampal volume/intracranial volume ratio [HpVR]) across AD stages.

Methods: The sample included 379 healthy participants, 694 participants with amnestic mild cognitive impairment (aMCI), and 235 participants with AD and dementia from the Alzheimer's Disease Neuroimaging Initiative who completed the Rey Auditory Verbal Learning Test (RAVLT). Cross-sectional analyses were conducted using linear regression to examine the interaction between sex and HpVR on RAVLT across and within diagnostic groups adjusting for age, education, and APOE ε4 status.

Results: Across groups, there were significant sex × HpVR interactions for immediate and delayed recall (p < 0.01). Women outperformed men among individuals with moderate to larger HpVR, but not among individuals with smaller HpVR. In diagnosis-stratified analyses, the HpVR × sex interaction was significant in the aMCI group, but not in the control or AD dementia groups, for immediate and delayed recall (p < 0.01). Among controls, women outperformed men on both outcomes irrespective of HpVR (p < 0.001). In AD dementia, better RAVLT performance was independently associated with female sex (immediate, p = 0.04) and larger HpVR (delayed, p = 0.001).

Conclusion: Women showed an advantage in verbal memory despite evidence of moderate hippocampal atrophy. This advantage may represent a sex-specific form of cognitive reserve delaying verbal memory decline until more advanced disease stages.

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Figures

**Figure 1. Relationship between hippocampal volume/intracranial volume ratio (HpVR) and Rey Auditory Verbal Learning Test (RAVLT) immediate recall scores in men and women**
RAVLT immediate recall scores as a function of HpVR (hippocampal/intracranial volume × 10³) and sex in the (A) overall group, (B) controls, (C) amnestic mild cognitive impairment (aMCI), and (D) Alzheimer disease (AD) dementia. β = sex-specific standardized regression coefficient of the relationship between RAVLT scores and HpVR controlling for age, education, *APOE*4, and diagnosis (overall sample only); HpVR = hippocampal/intracranial volume × 10³.

**Figure 2. Relationship between hippocampal volume/intracranial volume ratio (HpVR) and Rey Auditory Verbal Learning Test (RAVLT) delayed recall scores in men and women**
RAVLT delayed recall scores as a function of HpVR (hippocampal/intracranial volume × 10³) and sex in the (A) overall group, (B) controls, (C) amnestic mild cognitive impairment (aMCI), and (D) Alzheimer disease (AD) dementia. β = sex-specific standardized regression coefficient of the relationship between RAVLT scores and HpVR controlling for age, education, *APOE*4, and diagnosis (overall sample only); HpVR = hippocampal/intracranial volume × 10³.

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Comment in

Sex differences in cognition: Does the "fairer sex" need a fairer test?
Sano M, Gandy S. Sano M, et al. Neurology. 2016 Apr 12;86(15):1364-1365. doi: 10.1212/WNL.0000000000002573. Epub 2016 Mar 16. Neurology. 2016. PMID: 26984948 No abstract available.

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References

1. Stern Y, Gurland B, Tatemichi TK, Tang MX, Wilder D, Mayeux R. Influence of education and occupation on the incidence of Alzheimer's disease. JAMA 1994;271:1004–1010. - PubMed
1. Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 2002;8:448–460. - PubMed
1. Stern Y, Zarahn E, Hilton HJ, Flynn J, DeLaPaz R, Rakitin B. Exploring the neural basis of cognitive reserve. J Clin Exp Neuropsychol 2003;25:691–701. - PubMed
1. Stern Y, Albert S, Tang MX, Tsai WY. Rate of memory decline in AD is related to education and occupation: cognitive reserve? Neurology 1999;53:1942–1947. - PubMed
1. Le Carret N, Auriacombe S, Letenneur L, Bergua V, Dartigues JF, Fabrigoule C. Influence of education on the pattern of cognitive deterioration in AD patients: the cognitive reserve hypothesis. Brain Cogn 2005;57:120–126. - PubMed

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[1] Stern Y, Gurland B, Tatemichi TK, Tang MX, Wilder D, Mayeux R. Influence of education and occupation on the incidence of Alzheimer's disease. JAMA 1994;271:1004–1010. - PubMed

[2] Stern Y, Gurland B, Tatemichi TK, Tang MX, Wilder D, Mayeux R. Influence of education and occupation on the incidence of Alzheimer's disease. JAMA 1994;271:1004–1010. - PubMed

[3] Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 2002;8:448–460. - PubMed

[4] Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 2002;8:448–460. - PubMed

[5] Stern Y, Zarahn E, Hilton HJ, Flynn J, DeLaPaz R, Rakitin B. Exploring the neural basis of cognitive reserve. J Clin Exp Neuropsychol 2003;25:691–701. - PubMed

[6] Stern Y, Zarahn E, Hilton HJ, Flynn J, DeLaPaz R, Rakitin B. Exploring the neural basis of cognitive reserve. J Clin Exp Neuropsychol 2003;25:691–701. - PubMed

[7] Stern Y, Albert S, Tang MX, Tsai WY. Rate of memory decline in AD is related to education and occupation: cognitive reserve? Neurology 1999;53:1942–1947. - PubMed

[8] Stern Y, Albert S, Tang MX, Tsai WY. Rate of memory decline in AD is related to education and occupation: cognitive reserve? Neurology 1999;53:1942–1947. - PubMed

[9] Le Carret N, Auriacombe S, Letenneur L, Bergua V, Dartigues JF, Fabrigoule C. Influence of education on the pattern of cognitive deterioration in AD patients: the cognitive reserve hypothesis. Brain Cogn 2005;57:120–126. - PubMed

[10] Le Carret N, Auriacombe S, Letenneur L, Bergua V, Dartigues JF, Fabrigoule C. Influence of education on the pattern of cognitive deterioration in AD patients: the cognitive reserve hypothesis. Brain Cogn 2005;57:120–126. - PubMed

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Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy

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Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy

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