APOE ε4-Allele in Middle-Aged and Older Autistic Adults: Associations with Verbal Learning and Memory
This publication is included in the Autistic Autism Scholarship Project. one author of this publication is identified as autistic in the project.
About the autistic author markerHarker, S. A., Al-Hassan, L., Huentelman, M. J., Braden, B. B., & Lewis, C. R. (2023). APOE ε4-Allele in Middle-Aged and Older Autistic Adults: Associations with Verbal Learning and Memory. International Journal of Molecular Sciences, 24(21), 15988. https://doi.org/10.3390/ijms242115988
This publication is integrated into AutiHub through:
Authors
Abstract
Autism spectrum disorder (ASD) is a neurodevelopmental disability and recent evidence suggests that autistic adults are more likely to develop Alzheimer’s disease (Alz) and other dementias compared to neurotypical (NT) adults. The ε4-allele of the Apolipoprotein E (APOE) gene is the strongest genetic risk factor for Alz and negatively impacts cognition in middle-aged and older (MA+) adults. This study aimed to determine the impact of the APOE ε4-allele on verbal learning and memory in MA+ autistic adults (ages 40–71 years) compared to matched NT adults. Using the Auditory Verbal Learning Test (AVLT), we found that ε4 carriers performed worse on short-term memory and verbal learning across diagnosis groups, but there was no interaction with diagnosis. In exploratory analyses within sex and diagnosis groups, only autistic men carrying APOE ε4 showed worse verbal learning (p = 0.02), compared to autistic men who were not carriers. Finally, the APOE ε4-allele did not significantly affect long-term memory in this sample. These findings replicate previous work indicating that the APOE ε4-allele negatively impacts short-term memory and verbal learning in MA+ adults and presents new preliminary findings that MA+ autistic men may be vulnerable to the effects of APOE ε4 on verbal learning. Future work with a larger sample is needed to determine if autistic women may also be vulnerable.
Bibliography cited by this reference
Cited references are imported from external metadata sources when they are available. The list may be partial.
Cited bibliography overview
These indicators describe the bibliography cited by this publication. An author name is counted each time it appears in one cited reference, so the same person can be counted more than once. Names not yet linked to an author already present in AutiHub are treated as unknown, not as non-autistic. Last computed: 19 Sep 2026 01:01.
- With a DOI
- 56
- Without a DOI, from raw bibliography text
- 5
- References with detected author names
- 58 / 62 (93.5%)
- Without detected author names
- 4
- Without a structured title
- 4
- Without a stable identifier
- 4
- References with raw author names still to review
- 4
- References with external metadata lookup issues
- 0
- From DOI or external metadata
- 679
- From validated raw bibliography text
- 0
- Raw names already validated
- 0
- Raw names still to review
- 8
-
Fritz-Georg Lehnhardt , Christine Michaela Falter , Astrid Gawronski , Kathleen Pfeiffer , Ralf Tepest , Jeremy Franklin et al. (2016). Sex-Related Cognitive Profile in Autism Spectrum Disorders Diagnosed Late in Life: Implications for the Female Autistic Phenotype . Journal of Autism and Developmental Disorders, 46(1), 139-154. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Joseph Piven , Peter Rabins , on behalf of the Autism‐in‐Older Adults Working Group (2011). Autism Spectrum Disorders in Older Adults: Toward Defining a Research Agenda . Journal of the American Geriatrics Society, 59(11), 2151-2155. Wiley.Crossref OpenAlex OpenCitations
-
Claire B. Klein , Goldie A. McQuaid , Rebecca A. Charlton , Laura Klinger , Gregory L. Wallace (2023). Self‐reported cognitive decline among middle and older age autistic adults . Autism Research, 16(3), 605-616. Wiley.Crossref OpenAlex OpenCitations
-
Alan S. Kaufman , Nadeen L. Kaufman (2014). Kaufman Brief Intelligence Test, Second Edition . Encyclopedia of Special Education. Wiley.OpenAlex
-
Holly Hodges , Casey Fealko , Neelkamal Soares (2020). Autism spectrum disorder: definition, epidemiology, causes, and clinical evaluation . Translational Pediatrics, 9(S1), S55-S65. AME Publishing Company.Crossref OpenAlex OpenCitations
-
Michael A. DeTure , Dennis W. Dickson (2019). The neuropathological diagnosis of Alzheimer’s disease . Molecular Neurodegeneration, 14(1), 32. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Marshal F. Folstein , Susan E. Folstein , Paul R. McHugh (1975). “Mini-mental state” . Journal of Psychiatric Research, 12(3), 189-198. Elsevier BV.Crossref OpenAlex OpenCitations
-
Janine M. LaSalle (2023). Epigenomic signatures reveal mechanistic clues and predictive markers for autism spectrum disorder . Molecular Psychiatry, 28(5), 1890-1901. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Roberto Canitano , Giacomo Vivanti (2007). Tics and Tourette syndrome in autism spectrum disorders . Autism, 11(1), 19-28. SAGE Publications.Crossref OpenAlex OpenCitations
-
Jessica Foraker , Steven P. Millard , Lesley Leong , Zachary Thomson , Sunny Chen , C. Dirk Keene et al. (2015). The APOE Gene is Differentially Methylated in Alzheimer’s Disease . Journal of Alzheimer's Disease, 48(3), 745-755. SAGE Publications.Crossref OpenAlex OpenCitations
-
(n.d.). Maenner, M. J. (2023, September 20). Prevalence and Characteristics of Autism Spectrum Disorder among Children Aged 8 Years—Autism and Developmental Disabilities Monitoring Network, 11 Sites, United States, 2020. MMWR Surveill Summ, Available online: https://wwwdev.cdc.gov/mmwr/volumes/72/ss/ss7202a1.htm .Type: OtherCrossref
-
for the Alzheimer’s Disease Neuroimaging Initiative , Jessica Z. K. Caldwell , Jody-Lynn Berg , Jeffrey L. Cummings , Sarah J. Banks (2017). Moderating effects of sex on the impact of diagnosis and amyloid positivity on verbal memory and hippocampal volume . Alzheimer's Research & Therapy, 9(1), 72. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Elen Gjevik , Sigmund Eldevik , Torill Fjæran-Granum , Eili Sponheim (2011). Kiddie-SADS Reveals High Rates of DSM-IV Disorders in Children and Adolescents with Autism Spectrum Disorders . Journal of Autism and Developmental Disorders, 41(6), 761-769. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
B. Blair Braden , Christopher J. Smith , Amiee Thompson , Tyler K. Glaspy , Emily Wood , Divya Vatsa et al. (2017). Executive function and functional and structural brain differences in middle‐age adults with autism spectrum disorder . Autism Research, 10(12), 1945-1959. Wiley.Crossref OpenAlex OpenCitations
-
Meng-Chuan Lai , Michael Lombardo , Amber Ruigrok , Bhismadev Chakrabarti , Sally J. Wheelwright , Bonnie Auyeung et al. (2012). Cognition in Males and Females with Autism: Similarities and Differences . PLoS ONE, 7(10), e47198. Public Library of Science (PLoS).Crossref OpenAlex OpenCitations
-
Giacomo Vivanti , Sha Tao , Kristen Lyall , Diana L. Robins , Lindsay Shea (2021). The prevalence and incidence of early‐onset dementia among adults with autism spectrum disorder . Autism Research, 14(10), 2189-2199. Wiley.Crossref OpenAlex OpenCitations
-
Lauren Walker , Leonidas Stefanis , Johannes Attems (2019). Clinical and neuropathological differences between Parkinson's disease, Parkinson's disease dementia and dementia with Lewy bodies – current issues and future directions . Journal of Neurochemistry, 150(5), 467-474. Wiley.Crossref OpenAlex OpenCitations
-
A. M. Saunders , W. J. Strittmatter , D. Schmechel , P. H. St. George-Hyslop , M. A. Pericak-Vance , S. H. Joo et al. (1993). Association of apolipoprotein E allele ϵ4 with late-onset familial and sporadic Alzheimer’s disease . Neurology, 43(8), 1467. Ovid Technologies (Wolters Kluwer Health).Crossref OpenAlex
-
Lisa A. Croen , Ousseny Zerbo , Yinge Qian , Maria L Massolo , Steve Rich , Stephen Sidney et al. (2015). The health status of adults on the autism spectrum . Autism, 19(7), 814-823. SAGE Publications.Crossref OpenAlex OpenCitations
-
Erin E. Sundermann , Pauline M. Maki , Leah H. Rubin , Richard B. Lipton , Susan Landau , Anat Biegon et al. (2016). Female advantage in verbal memory . Neurology, 87(18), 1916-1924. Ovid Technologies (Wolters Kluwer Health).Crossref OpenAlex OpenCitations
-
K.L. Raiford , Y. Shao , I.C. Allen , E.R. Martin , M.M. Menold , H.H. Wright et al. (2004). No association between the APOE gene and autism . American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 125B(1), 57-60. Wiley.Crossref OpenAlex OpenCitations
-
B. Blair Braden , Cory Riecken (2019). Thinning faster? Age-related cortical thickness differences in adults with autism spectrum disorder . Research in Autism Spectrum Disorders, 64, 31-38. Elsevier BV.Crossref OpenAlex OpenCitations
-
Brittany N. Hand , Amber M Angell , Lauren Harris , Laura Arnstein Carpenter (2020). Prevalence of physical and mental health conditions in Medicare-enrolled, autistic older adults . Autism, 24(3), 755-764. SAGE Publications.Crossref OpenAlex OpenCitations
-
Maarit Kangas , Raija Korpelainen , Irene Vikman , Lars Nyberg , Timo Jämsä (2015). Sensitivity and False Alarm Rate of a Fall Sensor in Long-Term Fall Detection in the Elderly . Gerontology, 61(1), 61-68. S. Karger AG.OpenAlex
-
(n.d.). Kumar, A., Sidhu, J., Goyal, A., and Tsao, J. W. (2023, September 20). Alzheimer Disease, Available online: http://www.ncbi.nlm.nih.gov/books/NBK499922/ .Type: OtherCrossref
-
Carina Tatiana Giunco , Adriana B. de Oliveira , Andréa B. Carvalho-Salles , Dorotéia S.R. Souza , Ana Elizabete Silva , Simone Secco da Rocha et al. (2009). Association between APOE polymorphisms and predisposition for autism . Psychiatric Genetics, 19(6), 338. Ovid Technologies (Wolters Kluwer Health).Crossref OpenAlex OpenCitations
-
Benoît Sauty , Stanley Durrleman (2023). Impact of sex and APOE-ε4 genotype on patterns of regional brain atrophy in Alzheimer's disease and healthy aging . Frontiers in Neurology, 14, 1161527-1161527. Frontiers Media SA.Crossref OpenAlex OpenCitations
-
Richard J. Caselli , Amylou C. Dueck , Dona E.C. Locke , Leslie Baxter , Bryan Woodruff , Yonas E. Geda (2015). Sex-Based Memory Advantages and Cognitive Aging: A Challenge to the Cognitive Reserve Construct? Journal of the International Neuropsychological Society, 21(2), 95-104. Cambridge University Press (CUP).Crossref OpenAlex OpenCitations
-
Muhammad Shahid Nadeem , Salman Hosawi , Sultan Alshehri , Mohammed M. Ghoneim , Syed Sarim Imam , Bibi Nazia Murtaza et al. (2021). Symptomatic, Genetic, and Mechanistic Overlaps between Autism and Alzheimer’s Disease . Biomolecules, 11(11), 1635. MDPI AG.Crossref OpenAlex OpenCitations
-
John R. Crawford , Paul H. Garthwaite (2007). Comparison of a single case to a control or normative sample in neuropsychology: Development of a Bayesian approach . Cognitive Neuropsychology, 24(4), 343-372. Informa UK Limited.Crossref OpenAlex OpenCitations
-
E. H. Corder , A. M. Saunders , W. J. Strittmatter , D. E. Schmechel , P. C. Gaskell , G. W. Small et al. (1993). Gene Dose of Apolipoprotein E Type 4 Allele and the Risk of Alzheimer's Disease in Late Onset Families . Science, 261(5123), 921-923. American Association for the Advancement of Science (AAAS).Crossref OpenAlex OpenCitations
-
Broc A. Pagni , Melissa J.M. Walsh , Edward Ofori , Kewei Chen , Georgia Sullivan , Jocelyn Alvar et al. (2022). Effects of age on the hippocampus and verbal memory in adults with autism spectrum disorder: Longitudinal versus cross‐sectional findings . Autism Research, 15(10), 1810-1823. Wiley.Crossref OpenAlex OpenCitations
-
Janine D. Flory , Stephen B. Manuck , Robert E. Ferrell , Christopher M. Ryan , Matthew F. Muldoon (2000). Memory performance and the apolipoprotein E polymorphism in a community sample of middle-aged adults . American Journal of Medical Genetics, 96(6), 707-711. Wiley.Type: Article DOI: 10.1002/1096-8628(20001204)96:6<707::aid-ajmg1>3.0.co;2-v OpenAlex: https://openalex.org/W2041334242Crossref OpenAlex OpenCitations
-
Melissa J.M. Walsh , Edward Ofori , Broc A. Pagni , Kewei Chen , Georgia Sullivan , B. Blair Braden (2022). Preliminary findings of accelerated visual memory decline and baseline brain correlates in middle-age and older adults with autism: The case for hippocampal free-water . Frontiers in Aging Neuroscience, 14, 1029166. Frontiers Media SA.Crossref OpenAlex OpenCitations
-
Erin E. Sundermann , Anat Biegon , Leah H. Rubin , Richard B. Lipton , Wenzhu Mowrey , Susan Landau et al. (2016). Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy . Neurology, 86(15), 1368-1376. Ovid Technologies (Wolters Kluwer Health).Crossref OpenAlex OpenCitations
-
Nobutsugu Hirono , Etsuro Mori , Yoshitaka Ikejiri , Toru Imamura , Tatsuo Shimomura , Mamoru Hashimoto et al. (1997). [Japanese version of the Neuropsychiatric Inventory--a scoring system for neuropsychiatric disturbance in dementia patients]. PubMed, 49(3), 266-71.Type: Article OpenAlex: https://openalex.org/W2058161128OpenAlex
-
A.M. Saunders , W.J. Strittmatter , D. Schmechel , P.H. St. George-Hyslop , M.A. Pericak-Vance , S.H. Joo et al. (2011). Association of apolipoprotein E allele ε4 with late-onset familial and sporadic Alzheimer's disease . Neurology, 77(10), 950-950. Ovid Technologies (Wolters Kluwer Health).Type: Article DOI: 10.1212/01.wnl.0000405291.74999.10 10.1212/wnl.43.8.1467OpenCitations
-
Gagan Joshi , Carter Petty , Janet Wozniak , Aude Henin , Ronna Fried , Maribel Galdo et al. (2010). The Heavy Burden of Psychiatric Comorbidity in Youth with Autism Spectrum Disorders: A Large Comparative Study of a Psychiatrically Referred Population . Journal of Autism and Developmental Disorders, 40(11), 1361-1370. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Ana-Caroline Raulin , Sydney V. Doss , Zachary A. Trottier , Tadafumi C. Ikezu , Guojun Bu , Chia-Chen Liu (2022). ApoE in Alzheimer’s disease: pathophysiology and therapeutic strategies . Molecular Neurodegeneration, 17(1), 72. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Mark E. McCaulley (2019). Autism spectrum disorder and mercury toxicity: use of genomic and epigenetic methods to solve the etiologic puzzle . Acta Neurobiologiae Experimentalis, 79(2), 113-125. The Nencki Institute of Experimental Biology, Polish Academy of Sciences.Crossref OpenAlex OpenCitations
-
U. Beinhoff , H. Tumani , J. Brettschneider , D. Bittner , M. W. Riepe (2008). Gender-specificities in Alzheimer's disease and mild cognitive impairment . Journal of Neurology, 255(1), 117-122. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Jason A. Brandon , Brandon C. Farmer , Holden C. Williams , Lance A. Johnson (2018). APOE and Alzheimer’s Disease: Neuroimaging of Metabolic and Cerebrovascular Dysfunction . Frontiers in Aging Neuroscience, 10, 180. Frontiers Media SA.Crossref OpenAlex OpenCitations
-
H Payami , S Zareparsi , K R Montee , G J Sexton , J A Kaye , T D Bird et al. (1996). Gender difference in apolipoprotein E-associated risk for familial Alzheimer disease: A possible clue to the higher incidence of Alzheimer disease in women . Am. J Hum. Genet., 58(4), 803.Type: Article OpenAlex: https://openalex.org/W2144924184Crossref OpenAlex
-
Owen A. Williams , Yang An , Nicole M. Armstrong , Andrea T. Shafer , Jessica Helphrey , Melissa Kitner‐Triolo et al. (2019). Apolipoprotein E ε4 allele effects on longitudinal cognitive trajectories are sex and age dependent . Alzheimer's & Dementia, 15(12), 1558-1567. Wiley.Crossref OpenAlex OpenCitations
-
Jeroen S. Kok , Ina J. Berg , Erik J.A. Scherder (2013). Special Care Units and Traditional Care in Dementia: Relationship with Behavior, Cognition, Functional Status and Quality of Life - A Review . Dementia and Geriatric Cognitive Disorders Extra, 3(1), 360-375. S. Karger AG.OpenAlex
-
Emily Simonoff , Andrew Pickles , Tony Charman , Susie Chandler , Tom Loucas , Gillian Baird (2008). Psychiatric Disorders in Children With Autism Spectrum Disorders: Prevalence, Comorbidity, and Associated Factors in a Population-Derived Sample . Journal of the American Academy of Child & Adolescent Psychiatry, 47(8), 921-929. Elsevier BV.Crossref OpenAlex OpenCitations
-
Andre Altmann , Lu Tian , Victor W. Henderson , Michael D. Greicius , Alzheimer's Disease Neuroimaging Initiative Investigators (2014). Sex modifies the APOE ‐related risk of developing Alzheimer disease . Annals of Neurology, 75(4), 563-573. Wiley.Crossref OpenAlex OpenCitations
-
Sheina Emrani , Hirra A. Arain , Cassandra DeMarshall , Tal Nuriel (2020). APOE4 is associated with cognitive and pathological heterogeneity in patients with Alzheimer’s disease: a systematic review . Alzheimer's Research & Therapy, 12(1), 141. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Sebastiaan T.M. Peek , Katrien G. Luijkx , Maurice D. Rijnaard , Marianne E. Nieboer , Claire S. van der Voort , Sil Aarts et al. (2016). Older Adults' Reasons for Using Technology while Aging in Place . Gerontology, 62(2), 226-237. S. Karger AG.OpenAlex
-
Fan Liu , Luba M. Pardo , Maaike Schuur , Pascual Sanchez-Juan , Aaron Isaacs , Kristel Sleegers et al. (2010). The apolipoprotein E gene and its age-specific effects on cognitive function . Neurobiology of Aging, 31(10), 1831-1833. Elsevier BV.Crossref OpenAlex OpenCitations
-
Erin E. Sundermann , My Tran , Pauline M. Maki , Mark W. Bondi , Alzheimer's Disease Neuroimaging Initiative (2018). Sex differences in the association between apolipoprotein E ε4 allele and Alzheimer's disease markers . Alzheimer's & Dementia: Diagnosis, Assessment & Disease Monitoring, 10(1), 438-447. Wiley.Crossref OpenAlex OpenCitations
-
Brandalyn C. Riedel , Paul M. Thompson , Roberta Diaz Brinton (2016). Age, APOE and sex: Triad of risk of Alzheimer’s disease . The Journal of Steroid Biochemistry and Molecular Biology, 160, 134-147. Elsevier BV.Crossref OpenAlex OpenCitations
-
Anne G. Lever , Hilde M. Geurts (2016). Psychiatric Co-occurring Symptoms and Disorders in Young, Middle-Aged, and Older Adults with Autism Spectrum Disorder . Journal of Autism and Developmental Disorders, 46(6), 1916-1930. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Nahid Zokaei , Kathrin Giehl , Annie Sillence , Matt J. Neville , Fredrik Karpe , Anna C. Nobre et al. (2017). Sex and APOE: A memory advantage in male APOE ε4 carriers in midlife . Cortex, 88, 98-105. Elsevier BV.Crossref OpenAlex OpenCitations
-
Paula Duarte-Guterman , Arianne Y. Albert , Cindy K. Barha , Liisa A.M. Galea , on behalf of the Alzheimer’s Disease Neuroimaging Initiative (2021). Sex influences the effects of APOE genotype and Alzheimer’s diagnosis on neuropathology and memory . Psychoneuroendocrinology, 129, 105248. Elsevier BV.Crossref OpenAlex OpenCitations
-
Simon L. Evans , Nicholas G. Dowell , Fenella Prowse , Naji Tabet , Sarah L. King , Jennifer M. Rusted (2020). Mid age APOE ε4 carriers show memory-related functional differences and disrupted structure-function relationships in hippocampal regions . Scientific Reports, 10(1), a3110. Springer Science and Business Media LLC.Crossref OpenAlex OpenCitations
-
Leslie Baxter , Ashley Nespodzany , Melissa J.M. Walsh , Emily Wood , Christopher J. Smith , B. Blair Braden (2019). The influence of age and ASD on verbal fluency networks . Research in Autism Spectrum Disorders, 63, 52-62. Elsevier BV.Crossref OpenAlex OpenCitations
-
Eleni A Demetriou , Karen L Pepper , Shin Ho Park , Elizabeth Pellicano , Yun Ju C Song , Sharon L Naismith et al. (2021). Autism spectrum disorder: An examination of sex differences in neuropsychological and self-report measures of executive and non-executive cognitive function . Autism, 25(8), 2223-2237. SAGE Publications.Crossref OpenAlex OpenCitations
-
(n.d.). Kaufman, A. S., and Kaufman, N. L. (2023, July 29). Kaufman Brief Intelligence Test|Second Edition. Available online: https://www.pearsonassessments.com/store/usassessments/en/Store/Professional-Assessments/Cognition-%26-Neuro/Non-Verbal-Ability/Kaufman-Brief-Intelligence-Test-%7C-Second-Edition/p/100000390.html .Type: OtherCrossref
-
Schmidt, M. (1996). Rey Auditory Verbal Learning Test: RAVLT: A handbook, Western Psychological Services.Type: OtherCrossref
-
Matthew J. Maenner , Kelly A. Shaw , Amanda V. Bakian , Deborah A. Bilder , Maureen S. Durkin , Amy Esler et al. (2021). Prevalence and Characteristics of Autism Spectrum Disorder Among Children Aged 8 Years — Autism and Developmental Disabilities Monitoring Network, 11 Sites, United States, 2018 . MMWR. Surveillance Summaries, 70(11), 1-16. Centers for Disease Control MMWR Office.OpenAlex
-
Matthew J. Maenner , Zachary Warren , Ashley Robinson Williams , Esther Amoakohene , Amanda V. Bakian , Deborah A. Bilder et al. (2023). Prevalence and Characteristics of Autism Spectrum Disorder Among Children Aged 8 Years — Autism and Developmental Disabilities Monitoring Network, 11 Sites, United States, 2020 . MMWR. Surveillance Summaries, 72(2), 1-14. Centers for Disease Control MMWR Office.OpenAlex