Semantic Intrusion Errors Overcome the Impact of Literacy and Educational Attainment in Black/African Americans with and without Mild Cognitive Impairment
The Loewenstein-Acevedo Scale for Semantic Interference and Learning (LASSI-L) is a novel test of learning and inability to recover from proactive interference. It has been successfully employed with older adults at risk for cognitive impairment but the association between literacy, educational achievement, and LASSI-L performance in underserved Black/African American (B/AA) older adults remains unknown. 83 participants were evaluated as part of a longitudinal observational study to render a consensus diagnosis based on comprehensive clinical history and neuropsychological evaluation. Participants were classified into two groups: 43 were diagnosed with amnestic mild cognitive impairment (aMCI) and 40 were cognitively unimpaired (CU). The Wide Range Achievement Test-IV (WRAT-IV) was used to determine levels of literacy. Participants completed the LASSI-L, an AD sensitive cognitive challenge test which was not utilized for diagnosis to avoid circularity. The CU group outperformed the aMCI group across all LASSI-L measures after demographic covariate adjustment. Robust associations were found between education, literacy, and correct responses on different LASSI-L word lists (but not semantic intrusion errors). In contrast, aMCI participants largely exhibited no associations between LASSI-L indices and literacy effects. Stepwise logistic regression achieved an overall accuracy of 81% in classifying cognitive status (84% CU specificity, 71% aMCI sensitivity). Literacy was related to certain LASSI-L measures of learning in CU participants, but not among individuals with aMCI. Even when adjusting for demographic covariates, the LASSI-L effectively distinguished B/AA CU and aMCI groups. Results underscore the practicality of the LASSI-L to assess cognitive impairment in individuals with lower literacy proficiency, as our model correctly distinguish 84% of cognitively unimpaired individuals and 71% of individuals with amnestic mild cognitive impairment.
References
[1]
Aiken Morgan, A.T., Sims, R.C. and Whitfield, K.E. (2010) Cardiovascular Health and Education as Sources of Individual Variability in Cognitive Aging among African Americans. JournalofAgingandHealth, 22, 477-503. https://doi.org/10.1177/0898264310361627
[2]
Dotson, V.M., Kitner-Triolo, M.H., Evans, M.K. and Zonderman, A.B. (2009) Effects of Race and Socioeconomic Status on the Relative Influence of Education and Literacy on Cognitive Functioning. JournaloftheInternationalNeuropsychologicalSociety, 15, 580-589. https://doi.org/10.1017/s1355617709090821
[3]
Gupta, V.K., Winter, M., Cabral, H., Henault, L., Waite, K., Hanchate, A., et al. (2016) Disparities in Age-Associated Cognitive Decline between African-American and Caucasian Populations: The Roles of Health Literacy and Education. JournaloftheAmericanGeriatricsSociety, 64, 1716-1723. https://doi.org/10.1111/jgs.14257
[4]
Maher, C. and Calia, C. (2021) The Effect of Illiteracy on Performance in Screening Tools for Dementia: A Meta-Analysis. JournalofClinicalandExperimentalNeuropsychology, 43, 945-966. https://doi.org/10.1080/13803395.2022.2040433
[5]
Manly, J.J., Jacobs, D.M., Touradji, P., Small, S.A. and Stern, Y. (2002) Reading Level Attenuates Differences in Neuropsychological Test Performance between African American and White Elders. JournaloftheInternationalNeuropsychologicalSociety, 8, 341-348. https://doi.org/10.1017/s1355617702813157
[6]
Morgan, A.A., Marsiske, M. and Whitfield, K.E. (2007) Characterizing and Explaining Differences in Cognitive Test Performance between African American and European American Older Adults. ExperimentalAgingResearch, 34, 80-100. https://doi.org/10.1080/03610730701776427
[7]
Vadikolias, K., Tsiakiri-Vatamidis, A., Tripsianis, G., Tsivgoulis, G., Ioannidis, P., Serdari, A., et al. (2012) Mild Cognitive Impairment: Effect of Education on the Verbal and Nonverbal Tasks Performance Decline. BrainandBehavior, 2, 620-627. https://doi.org/10.1002/brb3.88
[8]
Katzman, R. (1993) Education and the Prevalence of Dementia and Alzheimer’s Disease. Neurology, 43, 13-20. https://doi.org/10.1212/wnl.43.1_part_1.13
[9]
Stern, Y., Alexander, G.E., Prohovnik, I. and Mayeux, R. (1992) Inverse Relationship between Education and Parietotemporal Perfusion Deficit in Alzheimer’s Disease. AnnalsofNeurology, 32, 371-375. https://doi.org/10.1002/ana.410320311
[10]
Stern, Y., Tang, M.X., Denaro, J. and Mayeux, R. (1995) Increased Risk of Mortality in Alzheimer’s Disease Patients with More Advanced Educational and Occupational Attainment. AnnalsofNeurology, 37, 590-595. https://doi.org/10.1002/ana.410370508
[11]
Friedland, R.P., Fritsch, T., Smyth, K.A., Koss, E., Lerner, A.J., Chen, C.H., et al. (2001) Patients with Alzheimer’s Disease Have Reduced Activities in Midlife Compared with Healthy Control-Group Members. ProceedingsoftheNationalAcademyofSciences, 98, 3440-3445. https://doi.org/10.1073/pnas.061002998
[12]
Manly, J.J., Schupf, N., Tang, M. and Stern, Y. (2005) Cognitive Decline and Literacy among Ethnically Diverse Elders. JournalofGeriatricPsychiatryandNeurology, 18, 213-217. https://doi.org/10.1177/0891988705281868
[13]
de Resende, E.d.P.F., Xia, F., Sidney, S., Launer, L.J., Schreiner, P.J., Erus, G., et al. (2022) Higher Literacy Is Associated with Better White Matter Integrity and Cognition in Middle Age. Alzheimer’s&Dementia: Diagnosis, Assessment&DiseaseMonitoring, 14, e12363. https://doi.org/10.1002/dad2.12363
[14]
Sachs-Ericsson, N. (2005) Racial Differences in Cognitive Decline in a Sample of Community-Dwelling Older Adults: The Mediating Role of Education and Literacy. AmericanJournalofGeriatricPsychiatry, 13, 968-975. https://doi.org/10.1176/appi.ajgp.13.11.968
[15]
Wright, R.S., Waldstein, S.R., Gerassimakis, C.S., Sprung, M.R., Moody, D.L.B., Taylor, A.D., et al. (2019) Multiple Influences on Cognitive Function among Urban-Dwelling African Americans. JournalofRacialandEthnicHealthDisparities, 6, 851-860. https://doi.org/10.1007/s40615-019-00584-x
[16]
Whitfield, K.E., Weidner, G., Clark, R. and Anderson, N.B. (2002) Sociodemographic Diversity and Behavioral Medicine. JournalofConsultingandClinicalPsychology, 70, 463-481. https://doi.org/10.1037//0022-006x.70.3.463
[17]
Lezak, M.D., Howieson, D.B., Bigler, E.D. and Tranel, D. (2012) Neuropsychological Assessment. 5th Edition, Oxford University Press.
[18]
Lee, S.D., Stucky, B.D., Lee, J.Y., Rozier, R.G. and Bender, D.E. (2010) Short Assessment of Health Literacy—Spanish and English: A Comparable Test of Health Literacy for Spanish and English Speakers. HealthServicesResearch, 45, 1105-1120. https://doi.org/10.1111/j.1475-6773.2010.01119.x
[19]
Miles, T.P. (2001) Dementia, Race, and Education: A Cautionary Note for Clinicians and Researchers. JournaloftheAmericanGeriatricsSociety, 49, 490. https://doi.org/10.1046/j.1532-5415.2001.49098.x
[20]
Manly, J.J., Jacobs, D.M., Sano, M., Bell, K., Merchant, C.A., Small, S.A., et al. (1998) Cognitive Test Performance among Nondemented Elderly African Americans and Whites. Neurology, 50, 1238-1245. https://doi.org/10.1212/wnl.50.5.1238
[21]
Werry, A.E., Daniel, M. and Bergström, B. (2019) Group Differences in Normal Neuropsychological Test Performance for Older Non-Hispanic White and Black/African American Adults. Neuropsychology, 33, 1089-1100. https://doi.org/10.1037/neu0000579
[22]
Kiselica, A.M., Johnson, E., Lewis, K. and Trout, K. (2021) Examining Misdiagnosis of Mild Cognitive Impairment among Black/African American Older Adults. Alzheimer’s&Dementia, 17, 2002-2011. https://doi.org/10.1002/alz.049776
[23]
Hanushek, E.A. and Woessmann, L. (2015) The Knowledge Capital of Nations: Education and the Economics of Growth. MIT Press.
[24]
Reardon, S.F. and Portilla, X.A. (2016) Recent Trends in Racial/Ethnic and Socio-economic Academic Achievement Gaps. AnnualReviewofSociology, 42, 351-370.
[25]
Ahl, R., Beiser, A., Au, R., et al. (2013) Defining MCI in the Framingham Heart Study Off-Spring. Neurology, 80, 1227-1233.
[26]
Sayegh, P., Arentoft, A., Thaler, N.S., Dean, A.C. and Thames, A.D. (2014) Quality of Education Predicts Performance on the Wide Range Achievement Test-4th Edition Word Reading Subtest. Archives of Clinical Neuropsychology, 29, 731-738.
[27]
Matías-Guiu, J.A., Curiel, R.E., Rognoni, T., Valles-Salgado, M., Fernández-Matar-rubia, M., Hariramani, R., et al. (2016) Validation of the Spanish Version of the LASSI-L for Diagnosing Mild Cognitive Impairment and Alzheimer’s Disease. JournalofAlzheimer’sDisease, 56, 733-742. https://doi.org/10.3233/jad-160866
[28]
Curiel Cid, R.E., Loewenstein, D.A., Rosselli, M., Matias-Guiu, J.A., Piña, D., Adjouadi, M., et al. (2019) A Cognitive Stress Test for Prodromal Alzheimer’s Disease: Multiethnic Generalizability. Alzheimer’s & Dementia: Diagnosis, Assessment & DiseaseMonitoring, 11, 550-559. https://doi.org/10.1016/j.dadm.2019.05.003
[29]
Capp, K.E., Curiel Cid, R.E., Crocco, E.A., Stripling, A., Kitaigorodsky, M., Sierra, L.A., et al. (2019) Semantic Intrusion Error Ratio Distinguishes between Cognitively Impaired and Cognitively Intact African American Older Adults. Journal of Alzheimer’sDisease, 73, 785-790. https://doi.org/10.3233/jad-191022
American Psychiatric Association (2022) Diagnostic and Statistical Manual of Mental Disorders. 5th Edition, American Psychiatric Publishing.
[32]
Besser, L., Kukull, W., Knopman, D.S., Chui, H., Galasko, D., Weintraub, S., et al. (2018) Version 3 of the National Alzheimer’s Coordinating Center’s Uniform Data Set. AlzheimerDisease&AssociatedDisorders, 32, 351-358. https://doi.org/10.1097/wad.0000000000000279
[33]
Wilkinson, G.S. and Robertson, G.J. (2006) Wide Range Achievement Test, Fourth Edition: Professional Manual. Psychological Assessment Resources.
[34]
Brandt, J. and Benedict, R.H.B. (2001) Hopkins Verbal Learning Test-Revised: Professional Manual. Psychological Assessment Resources.
[35]
Curiel, R. (2013) A New Scale for the Evaluation of Proactive and Retroactive Interference in Mild Cognitive Impairment and Early Alzheimer’s Disease. JournalofAgingScience, 1, Article No. 102.
[36]
Loewenstein, D.A., Acevedo, A., Agron, J. and Duara, R. (2007) Vulnerability to Proactive Semantic Interference and Progression to Dementia among Older Adults with Mild Cognitive Impairment. DementiaandGeriatricCognitiveDisorders, 24, 363-368. https://doi.org/10.1159/000109151
[37]
Curiel, R.E., Crocco, E.A., Raffo, A., Guinjoan, S.M., Nemeroff, C., Penate, A., et al. (2018) Failure to Recover from Proactive Semantic Interference Differentiates Amnestic Mild Cognitive Impairment and PreMCI from Normal Aging after Adjusting for Initial Learning Ability. AdvancesinAlzheimer’sDisease, 7, 50-61. https://doi.org/10.4236/aad.2018.72004
[38]
Crocco, E., Curiel, R.E., Acevedo, A., Czaja, S.J. and Loewenstein, D.A. (2014) An Evaluation of Deficits in Semantic Cueing and Proactive and Retroactive Interference as Early Features of Alzheimer’s Disease. TheAmericanJournalofGeriatricPsychiatry, 22, 889-897. https://doi.org/10.1016/j.jagp.2013.01.066
[39]
Loewenstein, D.A., Curiel, R.E., DeKosky, S., Rosselli, M., Bauer, R., Grieg-Custo, M., et al. (2017) Recovery from Proactive Semantic Interference and MRI Volume: A Replication and Extension Study. JournalofAlzheimer’sDisease, 59, 131-139. https://doi.org/10.3233/jad-170276
[40]
Zheng, D.D., Curiel Cid, R.E., Duara, R., Kitaigorodsky, M., Crocco, E. and Loewenstein, D.A. (2022) Semantic Intrusion Errors as a Function of Age, Amyloid, and Volumetric Loss: A Confirmatory Path Analysis. InternationalPsychogeriatrics, 34, 991-1001. https://doi.org/10.1017/s1041610220004007
[41]
Loewenstein, D.A., Curiel, R.E., Greig, M.T., Bauer, R.M., Rosado, M., Bowers, D., et al. (2016) A Novel Cognitive Stress Test for the Detection of Preclinical Alzheimer Disease: Discriminative Properties and Relation to Amyloid Load. TheAmericanJournalofGeriatricPsychiatry, 24, 804-813. https://doi.org/10.1016/j.jagp.2016.02.056
[42]
Loewenstein, D.A., Curiel, R.E., DeKosky, S., Bauer, R.M., Rosselli, M., Guinjoan, S.M., et al. (2018) Utilizing Semantic Intrusions to Identify Amyloid Positivity in Mild Cognitive Impairment. Neurology, 91, e976-e984. https://doi.org/10.1212/wnl.0000000000006128
[43]
Kitaigorodsky, M., Curiel Cid, R.E., Crocco, E., Gorman, K.L., González-Jiménez, C.J., Greig-Custo, M., et al. (2021) Changes in LASSI-L Performance over Time among Older Adults with Amnestic MCI and Amyloid Positivity: A Preliminary Study. JournalofPsychiatricResearch, 143, 98-105. https://doi.org/10.1016/j.jpsychires.2021.08.033
[44]
Loewenstein, D.A., Curiel, R.E., Duara, R. and Buschke, H. (2017) Novel Cognitive Paradigms for the Detection of Memory Impairment in Preclinical Alzheimer’s Disease. Assessment, 25, 348-359. https://doi.org/10.1177/1073191117691608
[45]
Torres, V.L., Rosselli, M., Loewenstein, D.A., Curiel, R.E., Vélez Uribe, I., Lang, M., et al. (2019) Types of Errors on a Semantic Interference Task in Mild Cognitive Impairment and Dementia. Neuropsychology, 33, 670-684. https://doi.org/10.1037/neu0000542
[46]
Curiel Cid, R.E., Crocco, E.A., Duara, R., Garcia, J.M., Rosselli, M., DeKosky, S.T., et al. (2020) A Novel Method of Evaluating Semantic Intrusion Errors to Distinguish between Amyloid Positive and Negative Groups on the Alzheimer’s Disease Continuum. JournalofPsychiatricResearch, 124, 131-136. https://doi.org/10.1016/j.jpsychires.2020.02.008
[47]
Cid, R.E.C. and Loewenstein, D.A. (2022) Salient Cognitive Paradigms to Assess Preclinical Alzheimer’s Disease. Neurotherapeutics, 19, 89-98. https://doi.org/10.1007/s13311-022-01192-0
[48]
Curiel Cid, R.E., Matias-Guiu, J.A. and Loewenstein, D.A. (2023) A Review of Novel Cognitive Challenge Tests for the Assessment of Preclinical Alzheimer’s Disease. Neuropsychology, 37, 661-672. https://doi.org/10.1037/neu0000883
