Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-14T07:25:27.112Z Has data issue: false hasContentIssue false

Subjective Cognitive Decline and its Relation to Verbal Memory and Sex in Cognitively Unimpaired Individuals from a Colombian Cohort with Autosomal-Dominant Alzheimer’s Disease

Published online by Cambridge University Press:  30 June 2021

Jairo E. Martinez
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA
Enmanuelle Pardilla-Delgado
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA
Edmarie Guzmán-Vélez
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA
Clara Vila-Castelar
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA
Rebecca Amariglio
Affiliation:
Department of Neurology, Center for Alzheimer Research and Treatment, Brigham, Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
Jennifer Gatchel
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA
Daniel C. Aguirre-Acevedo
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Medellin, Colombia
Yamile Bocanegra
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Medellin, Colombia
Ana Baena
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Medellin, Colombia
Eliana Henao
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Medellin, Colombia
Victoria Tirado
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Medellin, Colombia
Claudia Muñoz
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Medellin, Colombia
Margarita Giraldo-Chica
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Medellin, Colombia
Francisco Lopera
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Medellin, Colombia
Yakeel T. Quiroz*
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Medellin, Colombia Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA 02129, USA
*
*Correspondence and reprint requests to: Yakeel T. Quiroz, 100 First Ave, Building 39, Suite 101, Charlestown, MA 02129, USA. Tel: (617) 643-5944; Fax: (617) 643-5896. E-mail: [email protected]

Abstract

Objective:

Subjective Cognitive Decline (SCD) may be an early indicator of risk for Alzheimer’s disease (AD). Findings regarding sex differences in SCD are inconsistent. Studying sex differences in SCD within cognitively unimpaired individuals with autosomal-dominant AD (ADAD), who will develop dementia, may inform sex-related SCD variations in preclinical AD. We examined sex differences in SCD within cognitively unimpaired mutation carriers from the world’s largest ADAD kindred and sex differences in the relationship between SCD and memory performance.

Methods:

We included 310 cognitively unimpaired Presenilin-1 (PSEN-1) E280A mutation carriers (51% females) and 1998 noncarrier family members (56% females) in the study. Subjects and their study partners completed SCD questionnaires and the CERAD word list delayed recall test. ANCOVAs were conducted to examine group differences in SCD, sex, and memory performance. In carriers, partial correlations were used to examine associations between SCD and memory performance covarying for education.

Results:

Females in both groups had greater self-reported and study partner-reported SCD than males (all p < 0.001). In female mutation carriers, greater self-reported (p = 0.02) and study partner-reported SCD (p < 0.001) were associated with worse verbal memory. In male mutation carriers, greater self-reported (p = 0.03), but not study partner-reported SCD (p = 0.11) was associated with worse verbal memory.

Conclusions:

Study partner-reported SCD may be a stronger indicator of memory decline in females versus males in individuals at risk for developing dementia. Future studies with independent samples and preclinical trials should consider sex differences when recruiting based on SCD criteria.

Type
Research Article
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Acosta-Baena, N., Sepulveda-Falla, D., Lopera-Gómez, C. M., Jaramillo-Elorza, M. C., Moreno, S.,…Lopera, F. (2011). Pre-dementia clinical stages in presenilin 1 E280A familial early-onset Alzheimer’s disease: A retrospective cohort study. The Lancet. Neurology, 10(3), 213220. https://doi.org/10.1016/S1474-4422(10)70323-9 CrossRefGoogle ScholarPubMed
Afifi, M. (2007). Gender differences in mental health. Singapore Medical Journal, 48(5), 385391.Google ScholarPubMed
Aguirre-Acevedo, D. C., Gómez, R. D., Moreno, S., Henao-Arboleda, E., Motta, M., Muñoz, C., … Lopera, F. (2007). Validez y fiabilidad de la batería neuropsicológica CERAD-Col [Validity and reliability of the CERAD-Col neuropsychological battery]. Revista de neurologia, 45(11), 655660.CrossRefGoogle Scholar
Aguirre-Acevedo, D. C., Lopera, F., Henao, E., Tirado, V., Muñoz, C., Giraldo, M,…. Jaimes, F. (2016). Cognitive decline in a colombian kindred with autosomal dominant Alzheimer disease: A retrospective cohort study. JAMA Neurology, 73(4), 431438.CrossRefGoogle Scholar
Alzheimer’s disease facts and figures. (2020). Alzheimer’s & Dementia, 16(3), 391460. https://doi.org/10.1002/alz.12068 CrossRefGoogle Scholar
Ardila, A., Lopera, F., Rosselli, M., Moreno, S., Madrigal, L., Arango-Lasprilla, J. C., … Kosik, K. S. (2000). Neuropsychological profile of a large kindred with familial Alzheimer’s disease caused by the E280A single presenilin-1 mutation. Archives of Clinical Neuropsychology : The Official Journal of the National Academy of Neuropsychologists, 15(6), 515528.CrossRefGoogle ScholarPubMed
Benzinger, T. L. S., Blazey, T., Jack, C. R., Koeppe, R. A., Su, Y., Xiong, C., … Morris, J. C. (2013). Regional variability of imaging biomarkers in autosomal dominant Alzheimer’s disease. Proceedings of the National Academy of Sciences, 110(47), E4502E4509. https://doi.org/10.1073/pnas.1317918110 CrossRefGoogle ScholarPubMed
Brown, M. J., Hill, N. L., & Haider, M. R. (2020). Age and gender disparities in depression and subjective cognitive decline-related outcomes. Aging & Mental Health, 1–8. Advance online publication. https://doi.org/10.1080/13607863.2020.1861214 CrossRefGoogle Scholar
Buckley, R., Saling, M. M., Ames, D., Rowe, C. C., Lautenschlager, N. T., Macaulay, S. L., … Australian Imaging Biomarkers and Lifestyle Study of Aging (AIBL) Research Group (2013). Factors affecting subjective memory complaints in the AIBL aging study: Biomarkers, memory, affect, and age. International Psychogeriatrics, 25(8), 13071315. https://doi.org/10.1017/S1041610213000665 CrossRefGoogle ScholarPubMed
Buckley, R. F., Hanseeuw, B., Schultz, A. P., Vannini, P., Aghjayan, S. L., Properzi, M. J., … Amariglio, R. E. (2017). Region-specific association of subjective cognitive decline with tauopathy independent of global β-amyloid burden. JAMA Neurology, 74(12), 1455. https://doi.org/10.1001/jamaneurol.2017.2216 CrossRefGoogle ScholarPubMed
Buckley, R. F., Mormino, E. C., Amariglio, R. E., Properzi, M. J., Rabin, J. S., Lim, Y. Y., … Sperling, R. A. (2018). Sex, amyloid, and APOE ϵ4 and risk of cognitive decline in preclinical Alzheimer’s disease: Findings from three well-characterized cohorts. Alzheimer’s & Dementia, 14(9), 11931203. https://doi.org/10.1016/j.jalz.2018.04.010 CrossRefGoogle ScholarPubMed
Buckley, R. F., Mormino, E. C., Rabin, J. S., Hohman, T. J., Landau, S., Hanseeuw, B. J., … Sperling, R. A. (2019). Sex differences in the association of global amyloid and regional tau deposition measured by positron emission tomography in clinically normal older adults. JAMA Neurology, 76(5), 542. https://doi.org/10.1001/jamaneurol.2018.4693 CrossRefGoogle ScholarPubMed
Buckley, R. F., Sikkes, S., Villemagne, V. L., Mormino, E. C., Rabin, J. S., Burnham, S., … Amariglio, R. E. (2019). Using subjective cognitive decline to identify high global amyloid in community-based samples: A cross-cohort study. Alzheimer’s & Dementia: Diagnosis, Assessment & Disease Monitoring, 11(1), 670678. https://doi.org/10.1016/j.dadm.2019.08.004 Google ScholarPubMed
Call, J. B., & Shafer, K. (2018). Gendered manifestations of depression and help seeking among men. American Journal of Men’s Health, 12(1), 4151.CrossRefGoogle ScholarPubMed
Evans, J., Frank, B., Oliffe, J. L., & Gregory, D. (2011). Health, Illness, Men and Masculinities (HIMM): A theoretical framework for understanding men and their health. Journal of Men’s Health, 8(1), 715. https://doi.org/10.1016/j.jomh.2010.09.227 Google Scholar
Fagan, A. M., Xiong, C., Jasielec, M. S., Bateman, R. J., Goate, A. M., Benzinger, T. L. S., … Holtzman, D. M. (2014). Longitudinal change in CSF biomarkers in autosomal-dominant Alzheimer’s disease. Science Translational Medicine, 6(226), 226ra30226ra30. https://doi.org/10.1126/scitranslmed.3007901 CrossRefGoogle ScholarPubMed
Fiest, K. M., Roberts, J. I., Maxwell, C. J., Hogan, D. B., Smith, E. E., Frolkis, A., … Jetté, N. (2016). The prevalence and incidence of dementia due to Alzheimer’s disease: A systematic review and meta-analysis. Canadian Journal of Neurological Sciences/Journal Canadien Des Sciences Neurologiques, 43(S1), S51S82. https://doi.org/10.1017/cjn.2016.36 CrossRefGoogle ScholarPubMed
Fleisher, A. S., Chen, K., Quiroz, Y. T., Jakimovich, L. J., Gomez, M. G., Langois, C. M., … Reiman, E. M. (2012). Florbetapir PET analysis of amyloid-β deposition in the presenilin 1 E280A autosomal dominant Alzheimer’s disease kindred: A cross-sectional study. The Lancet Neurology, 11(12), 10571065. https://doi.org/10.1016/S1474-4422(12)70227-2 CrossRefGoogle ScholarPubMed
Folstein, M. F., Robins, L. N., & Helzer, J. E. (1983). The Mini-Mental State Examination. Archives of General Psychiatry, 40(7), 812. https://doi.org/10.1001/archpsyc.1983.01790060110016 CrossRefGoogle ScholarPubMed
Fuller, J. T., Cronin-Golomb, A., Gatchel, J. R., Norton, D. J., Guzmán-Vélez, E., Jacobs, H., … Quiroz, Y. T. (2019). Biological and cognitive markers of presenilin1 E280A autosomal dominant Alzheimer’s disease: A comprehensive review of the colombian kindred. Journal of Prevention of Alzheimer’s Disease, 6(2), 112120. https://doi.org/10.14283/jpad.2019.6 Google ScholarPubMed
Gatchel, J. R., Lopera, F., Norton, D. J., Baena, A., Guzman-Velez, E., Sanchez, J. S., … Quiroz, Y. T. (2020). Association of subjective cognitive decline with markers of brain pathology in preclinical autosomal dominant Alzheimer’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 91(3), 330332. https://doi.org/10.1136/jnnp-2019-321205 CrossRefGoogle ScholarPubMed
Gatchel, J. R., Rabin, J. S., Buckley, R. F., Locascio, J. J., Quiroz, Y. T., Yang, H.-S….Harvard Aging Brain Study. (2019). Longitudinal association of depression symptoms with cognition and cortical amyloid among community-dwelling older adults. JAMA Network Open, 2(8), e198964e198964.CrossRefGoogle ScholarPubMed
Heser, K., Kleineidam, L., Wiese, B., Oey, A., Roehr, S., Pabst, A., … Wagner, M. (2019). Subjective cognitive decline may be a stronger predictor of incident dementia in women than in men. Journal of Alzheimer’s Disease, 68(4), 14691478.CrossRefGoogle ScholarPubMed
Holmen, J., Langballe, E. M., Midthjell, K., Holmen, T. L., Fikseaunet, A., Saltvedt, I., & Tambs, K. (2013). Gender differences in subjective memory impairment in a general population: The HUNT study, Norway. BMC Psychology, 1(1), 19. https://doi.org/10.1186/2050-7283-1-19 CrossRefGoogle Scholar
Jessen, F., Amariglio, R. E., Buckley, R. F., van der Flier, W. M., Han, Y., Molinuevo, J. L., … Wagner, M. (2020). The characterisation of subjective cognitive decline. The Lancet Neurology, 19(3), 271278. https://doi.org/10.1016/S1474-4422(19)30368-0 CrossRefGoogle ScholarPubMed
Mielke, M. M. (2018). Sex and gender differences in Alzheimer’s disease dementia. The Psychiatric Times, 35(11), 1417.Google ScholarPubMed
Niu, H., Álvarez-Álvarez, I., Guillén-Grima, F., & Aguinaga-Ontoso, I. (2017). Prevalence and incidence of Alzheimer’s disease in Europe: A meta-analysis. Neurología (English Edition), 32(8), 523532. https://doi.org/10.1016/j.nrleng.2016.02.009 CrossRefGoogle ScholarPubMed
Norton, D. J., Amariglio, R., Protas, H., Chen, K., & Aguirre, D. C. (2017). Subjective memory complaints in preclinical autosomal dominant Alzheimer disease. Neurology, 89(14), 14641470.CrossRefGoogle ScholarPubMed
Paradise, M. B., Glozier, N. S., Naismith, S. L., Davenport, T. A., & Hickie, I. B. (2011). Subjective memory complaints, vascular risk factors and psychological distress in the middle-aged: A cross-sectional study. BMC Psychiatry, 11(1), 108. https://doi.org/10.1186/1471-244X-11-108 CrossRefGoogle ScholarPubMed
Pearman, A., & Storandt, M. (2004). Predictors of subjective memory in older adults. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 59(1), P4P6. https://doi.org/10.1093/geronb/59.1.p4 CrossRefGoogle ScholarPubMed
Pérès, K., Helmer, C., Amieva, H., Matharan, F., Carcaillon, L., Jacqmin-Gadda, H., … Dartigues, J.-F. (2011). Gender differences in the prodromal signs of dementia: Memory complaint and IADL-restriction. A prospective population-based cohort. Journal of Alzheimer’s Disease, 27(1), 3947. https://doi.org/10.3233/JAD-2011-110428 CrossRefGoogle ScholarPubMed
Plassman, B. L., Langa, K. M., Fisher, G. G., Heeringa, S. G., Weir, D. R., Ofstedal, M. B., … Wallace, R. B. (2007). Prevalence of dementia in the United States: The aging, demographics, and memory study. Neuroepidemiology, 29(1–2), 125132. https://doi.org/10.1159/000109998 CrossRefGoogle ScholarPubMed
Rabin, L. A., Smart, C. M., Crane, P. K., Amariglio, R. E., Berman, L. M., Boada, M.,…Sikkes, S. A. (2015). Subjective cognitive decline in older adults: An overview of self-report measures used across 19 international research studies. Journal of Alzheimer’s Disease, 48, S63S86. https://doi.org/10.3233/JAD-150154 CrossRefGoogle Scholar
Reisberg, B., Ferris, S. H., de Leon, M. J., & Crook, T. (1982). The Global Deterioration Scale for assessment of primary degenerative dementia. American Journal of Psychiatry, 139(9), 11361139. https://doi.org/10.1176/ajp.139.9.1136 Google ScholarPubMed
Rusticus, S. A., & Lovato, C. Y. (2014.). Impact of sample size and variability on the power and type I error rates of equivalence tests: A simulation study. Practical Assessment, Research, and Evaluation https://doi.org/10.7275/4S9M-4E81 CrossRefGoogle Scholar
Sclan, S., & Reisberg, B. (1992). Functional Assessment Staging (FAST) in Alzheimer’s disease: Reliability, validity, and ordinality. International Psychogeriatrics, 4(3), 5569.CrossRefGoogle ScholarPubMed
Sundermann, E. E., Edmonds, E. C., Delano-Wood, L., Galasko, D. R., Salmon, D. P., Rubin, L. H., & Bondi, M. W. (2018). Sex influences the accuracy of subjective memory complaint reporting in older adults. Journal of Alzheimer’s Disease, 61(3), 11631178. https://doi.org/10.3233/JAD-170425 CrossRefGoogle ScholarPubMed
Thompson, A. E., Anisimowicz, Y., Miedema, B., Hogg, W., Wodchis, W. P., & Aubrey-Bassler, K. (2016). The influence of gender and other patient characteristics on health care-seeking behaviour: A QUALICOPC study. BMC Family Practice, 17(1), 38. https://doi.org/10.1186/s12875-016-0440-0 CrossRefGoogle ScholarPubMed
Vannini, P., Hanseeuw, B. J., Gatchel, J. R., Sikkes, S. A. M., Alzate, D., Zuluaga, Y..…Quiroz, Y. T. (2020). Trajectory of unawareness of memory decline in individuals with autosomal dominant Alzheimer disease. JAMA Network Open, 3(12), e2027472e2027472. https://doi.org/10.1001/jamanetworkopen.2020.27472 CrossRefGoogle ScholarPubMed
Vila-Castelar, C., Guzmán-Vélez, E., Pardilla-Delgado, E., Buckley, R. F., Bocanegra, Y., Baena, A.,…Quiroz, Y. T. (2020). Examining sex differences in markers of cognition and neurodegeneration in autosomal dominant Alzheimer’s disease: Preliminary findings from the Colombian Alzheimer’s prevention initiative biomarker study. Journal of Alzheimer’s Disease, 77(4), 17431753. https://doi.org/10.3233/JAD-200723 CrossRefGoogle ScholarPubMed
Welch, B. L. (1947). The generalization of ‘Student’s’ problem when several different population variances are involved. Biometrika, 34(1/2), 2835. https://doi.org/10.2307/2332510 Google Scholar
Wool, C. A., & Barsky, A. J. (1994). Do women somatize more than men? Psychosomatics, 35(5), 445452. https://doi.org/10.1016/S0033-3182(94)71738-2 CrossRefGoogle ScholarPubMed