Cited by 318Dementia and Cognitive Impairment ResearchHistorical and Modern Theater StudiesNeurobiology of Language and Bilingualism

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Longitudinal Verbal Fluency in Normal Aging, Preclinical, and Prevalent Alzheimer’s Disease

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Clark, Linda J., Gatz, Margaret, Zheng, Ling, Chen, Yu-Ling, McCleary, Carol, Mack, Wendy J.·2009·American Journal of Alzheimer's Disease & Other Dementias®

DOI 10.1177/1533317509345154PMC PMC2824246

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Abstract

Background: Few longitudinal studies evaluate differences in patterns of change of category compared to letter fluency across the spectrum of cognitive impairment. Methods: We compared change in category (animal and supermarket) and letter (F, A, S) fluency among 239 participants in 3 groups: remained cognitively normal throughout follow-up (n = 96), developed Alzheimer’s Disease (AD; preclinical AD, n = 21), and with AD at initial testing (prevalent AD, n = 122). Results: At baseline, prevalent and preclinical AD groups scored lower on animal than letter fluency. On all fluency measures, the prevalent AD declined faster than other groups (all P < .0001), and preclinical AD declined faster than unimpaired (all P ≤ .02). Overall, animal fluency declined faster than letter fluency; animal fluency declined significantly faster than letter fluency among cognitively normal and prevalent AD participants. Conclusion: Greater longitudinal declines in category compared to letter fluency are consistent with cross-sectional studies. Steeper declines on both fluency measures distinguish preclinical AD from cognitively unimpaired individuals.

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Applied Longitudinal Data Analysis: Modeling Change and Event Occurrence
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“group, given the relative stability of semantic memory in normal aging.(22) First, it is difficult to separate normal aging from disease.”
Background
Mild cognitive impairment can be distinguished from Alzheimer disease and normal aging for clinical trials
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“It has further been shown that category fluency distinguishes normal controls from participants diagnosed as either cognitively impaired but not demented (CIND) or as mild cognitive impairment (MCI).(9,10) Finally, baseline impairments in category fluency predict who subsequently will develop AD.”
Background
Verbal fluency performance in dementia of the Alzheimer’s type: a meta-analysis
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“Tests of verbal fluency draw on both executive function and language abilities, and provide good discrimination between persons with normal cognitive function compared to those with mild Alzheimer’s disease (AD).(1) Although tests of verbal fluency can include either category fluency or letter fluency, it is now well…”
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Comparisons of Verbal Fluency Tasks in the Detection of Dementia of the Alzheimer Type
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“Our findings are consistent with the suggestion that the preclinical individuals may already have deterioration in the temporal/parietal area, since animal naming would be associated with the temporal/parietal part of the brain, while FAS would be associated with the frontal lobes.(20,21) We add 2 further comments abo…”
Result
Language performance in Alzheimer's disease and mild cognitive impairment: A comparative review
Taler, V., & Phillips, N. A. (2008) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803390701550128 · Cited by 529 · cited 1×
“Our cross-sectional findings are consistent with numerous reports that have compared fluency measures at a single testing between participants with AD and unimpaired participants(1-7) and between participants with MCI or preclinical AD and unimpaired participants.(2,9-12) In these cross-sectional analyses, we found th…”
Result
The 9 year cognitive decline before dementia of the Alzheimer type: a prospective population-based study
Amieva, H., Jacqmin‐Gadda, H., Orgogozo, J., Carret, N. L., Helmer, C., Letenneur, L., Barberger‐Gateau, P., Fabrigoule, C., & Dartigues, J. (2005) · Brain · doi:10.1093/brain/awh451 · Cited by 470 · cited 11×
“One study found that participants with AD showed more rapid decline at 1-year followup in category fluency compared to cognitively intact participants, while showing little change in letter fluency in the same time period.14 In the MoVIES study, there was significant decline over 2 years on categorical but not on lett…”
BackgroundInfluential

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Research works printed but not linked: 4

10.1212/01.WNL.0000147470.58328.50 · DOI · Paper page
10.1212/WNL.34.7.939 · DOI · Paper page
Singer JD, 2003, Modeling Change and Event Occurrence
10.1037/0882-7974.17.3.435 · DOI

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“The AF test challenges participants to generate as many animal names as possible within a minute, testing their verbal fluency and executive functioning, with each correct response earning a point (Clark et al., 2009).”
Background
Association between coffee intake and skeletal muscle mass among U.S. adults: a population-based study
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Increased serum methylmalonic acid levels were associated with the presence of cognitive dysfunction in older chronic kidney disease patients with albuminuria
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“The Animal Fluency (AF) test asked participants to name as many animals as they can in 1 min to assess verbal fluency [23].”
Background
Establishment, Prediction, and Validation of a Nomogram for Cognitive Impairment in Elderly Patients With Diabetes
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The Association between Peanut and Peanut Butter Consumption and Cognitive Function among Community-Dwelling Older Adults
Katzman, E. W., & Nielsen, S. (2021) · The journal of prevention of Alzheimer's disease · doi:10.14283/jpad.2021.32 · Cited by 8
“The AFT assesses categorical verbal fluency, a component of executive function and has been shown to differentiate between normal cognitive function, mild cognitive impairment, and more severe forms of cognitive impairment including Alzheimer’s disease (13-16).”
Edad, escolarización y tareas de fluencia verbal para el screening de pacientes con enfermedad de Alzheimer
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Cardiovascular disease attenuates the protective effect of folate on global cognitive function in an elderly population: a cross-sectional study
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What does “Internet” mean to us as we age? A multi-task investigation on the conceptualization of the technological domain across generations
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Associations between circadian alignment and cognitive functioning in a nationally representative sample of older adults
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“In addition, phonemic fluency is sensitive to subtle cognitive alterations that can indicate cognitive declining even in healthier stages (30).”
Background
O uso de testes de fluência verbal como ferramenta de rastreio cognitivo em idosos
Teldeschi, A., Perez, M., Sanchez, M. A., & Lourenço, R. A. (2018) · doi:10.12957/rhupe.2017.33289 · Cited by 7
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The Relationship between Leisure Time Physical Activity and Cognitive Function in Older Americans
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“The Animal Fluency test has been used in large-scale screenings and epidemiologic studies (27-29).”
Longitudinal Effects of Herpesviruses on Multiple Cognitive Outcomes in Healthy Elderly Adults
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Result
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“It should be noted that impairment on semantic fluency (when measured by naming animals) is a predictor of Alzheimer’s disease [52].”
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The Association Between the Atherogenic Index of Plasma and Cognitive Function: Evidence From the NHANES 2011–2014
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“For every animal that was named, one point was given (Clark et al. 2009).”
Trajectory of Cognitive Function After Incident Heart Failure
Shore, S., Li, H., Zhang, M., Whitney, R. T., Gross, A. L., Bhatt, A. S., Nallamothu, B. K., Giordani, B., Briceño, E. M., Sussman, J. B., et al. (2025) · Circulation Heart Failure · doi:10.1161/circheartfailure.124.011837 · Cited by 9
“44 In addition, progressive cognitive decline is associated with depression, 45 dementia, 46 and functional decline, 47 causing greater caregiver burden and institutionalization risk.”
Frequency and Early Predictors of Cognitive Deterioration in Amyotrophic Lateral Sclerosis: A Longitudinal Population‐Based Study
Iazzolino, B., Palumbo, F., Moglia, C., Manera, U., Grassano, M., Matteoni, E., Cabras, S., Brunetti, M., Vasta, R., Pagani, M., et al. (2025) · Annals of Neurology · doi:10.1002/ana.27194 · Cited by 5
Amyloid‐related changes in fluency in patients with subjective cognitive decline
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Application of the Semantic Fluency Test in the Screening of Mandarin-Chinese-Speaking Older Adults with Mild Dementia of the Alzheimer Type
Lin, M.-C., & Chih, Y.-C. (2023) · Behavioral Science · doi:10.3390/bs13080635 · Cited by 5
“[23], who assessed the performance of healthy older adults and patients with DAT in the animal fluency test.”
Background
Language processing in normal aging: Contributions of information-universal and information-specific factors
Hanlin, W. U., Zhou, Y. U., Xuejiao, W. A. N. G., & ZHANG, Q. (2020) · Acta Psychologica Sinica · doi:10.3724/sp.j.1041.2020.00541 · Cited by 7
“…−0.129 (0.225) 词汇理解 R² = 0.082*** ΔR² = 0.175*** R² = 0.282*** ΔR² = 0.034** R² = 0.351*** ΔR² = 0.001 ΔΔR² = 0.141 ΔΔR² = 0.033 性别 −0.009 (0.133) 0.162 (0.099) 0.138 (0.112) 0.186 (0.099) 0.117 (0.101) 0.160 (0.098) 受教育年限 0.371 (0.065)*** 0.043 (0.054) 0.140 (0.059)* 0.029 (0.054) 0.019…”
Influential
15-Year Secular Trends in Cognitive Function Among Older Adults in the United States
Frith, E., & Loprinzi, P. D. (2018) · Psychological Reports · doi:10.1177/0033294118765227 · Cited by 5
“The Animal Fluency test has also been employed in various epidemiological cohorts (Canning, Leach, Stuss, Ngo, & Black, 2004; Clark et al., 2009; Grundman et al., 2004; Ramirez-Gomez et al., 2017; Tuokko, Griffith, Simard, & Taler, 2017), assessing verbal fluency, a component of executive function (Duff, Schoenberg, S…”
Method
Improved conceptual generation and selection with transcranial direct current stimulation in older adults
Madden, D. L., Sale, M. V., & Robinson, G. A. (2018) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803395.2018.1491529 · Cited by 7
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Method
The Progression of Alzheimer's Disease Can Be Assessed with a Short Version of the CERAD Neuropsychological Battery: The Kuopio ALSOVA Study
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Neuromodulation Interventions for Language Deficits in Alzheimer’s Disease: Update on Current Practice and Future Developments
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The role of physical activity in preventing cognitive decline among U.S. older adults with diabetes and prediabetes: a cross-sectional study
Wang, Y., Liu, D., Wang, H., Wang, M., Ruan, W., Han, Y., & Han, Y. (2025) · Frontiers in Public Health · doi:10.3389/fpubh.2025.1603627 · Cited by 4
Association between age at first birth and cognitive function in women 60 years and older: the 2011–2014 cross-sectional National Health and Nutrition Examination Survey (NHANES) study
Zhao, J.-N., Deng, L., Sun, C., & Lin, M. (2025) · BMC Public Health · doi:10.1186/s12889-025-22767-4 · Cited by 3
A synergistic effect of secondhand smoke with vitamin D deficiency on cognitive impairment in older adults: a cross sectional study
Li, Y., Shen, Q., Chen, C., Yin, X., Wang, X.-R., Yang, X., Zhang, X., Chen, L., Xu, J., & Gong, G. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1533193 · Cited by 4
“Categorical verbal fluency in executive function was examined with the AFT, which has been demonstrated that scores can be used to differentiate individuals who have normal cognitive abilities from those with MCI and more severe cognitive impairments (21, 22).”
Functional near-infrared spectroscopy and vagus somatosensory evoked potentials add to the power of established parameters such as poor cognitive performance, dsyosmia and APOe genotype to predict cognitive decline over 8 years in the elderly
Herrmann, M. J., Wuttke, A., Breuninger, L., Eff, J., Ettlinger, S., Fischer, M., Götzelmann, A., Gram, A., Pomper, L. D., Schneider, E., et al. (2024) · Journal of Neural Transmission · doi:10.1007/s00702-024-02859-y · Cited by 4
“Prior studies have shown the predictive validity (sensitivity and specificity) of different cognitive measures for the development of AD such as associative learning (Ahmed et al. 2008 ) and verbal fluency (Clark et al. 2009).”
Associations of Handgrip Strength Weakness and Asymmetry with Lower Cognitive Function: Results from the National Health and Nutrition Examination Survey (2011–2014)
Peng, L., Xiang, Q., Zhou, Y. J., & Yin, R. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-231375 · Cited by 5

Authors: Clark, L. J., Gatz, M., Zheng, L., Chen, Y.-L., McCleary, C., & Mack, W. J.
Affiliations: University of Southern California (US)
Alzheimer Disease Research Center, and Department of Neurology, University of Southern California, Los Angeles, California
Corresponding author: Mack, Wendy J.
ORCID: Gatz, Margaret
Zheng, Ling
Mack, Wendy J.
Venue: American Journal of Alzheimer's Disease & Other Dementias®
Publisher: SAGE Publications
Published: 2009-09-16
Volume: 24
Issue: 6
Pages: 461-468
ISSN: 0888-4897 (ISSN-L)
1533-3175
1938-2731
DOI: 10.1177/1533317509345154
PMC: PMC2824246
OpenAlex: W2058044289
Cited by: 318
References: 24
Citations by year: 2026: 14 · 2025: 51 · 2024: 37 · 2023: 34 · 2022: 20 · 2021: 23 · 2020: 20 · 2019: 18 · 2018: 23 · 2017: 11 · 2016: 10 · 2015: 14 · 2014: 10 · 2013: 12 · 2012: 5
FWCI: 4.12
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)
Locations: American Journal of Alzheimer s Disease & Other Dementias® (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute on Aging (P50-AG05142, P50AG005142)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Social Sciences › Psychology › Clinical Psychology › Historical and Modern Theater Studies
Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
Keywords: verbal fluency, semantic fluency, phonemic fluency, animal fluency, Alzheimer's disease, preclinical Alzheimer's disease, normal aging, cognitive decline, longitudinal change, cognitive impairment
MeSH terms: Aged, Aged, 80 and over, Aging, Alzheimer Disease, Cognition, Cognition Disorders, Diagnosis, Differential, Female, Follow-Up Studies, Humans, Longitudinal Studies, Male, Memory, Neuropsychological Tests, Semantics, Speech Disorders, Prevalence, Multivariate Analysis, Disease Progression, Early Diagnosis

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Longitudinal Verbal Fluency in Normal Aging, Preclinical, and Prevalent Alzheimer’s Disease

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