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Cited by 65Dementia and Cognitive Impairment ResearchDiabetes Management and ResearchDiabetes Management and Education

Cognitive Function Deficits Associated With Long-Duration Type 1 Diabetes and Vascular Complications

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Musen, Gail, Tinsley, Liane J., Marcinkowski, Katrina A., Pober, David, Sun, Jennifer K., Khatri, Maya, Huynh, Richie, Lu, Annie +2 more·2018·Diabetes Care
DOI 10.2337/dc17-1955PMC PMC6054500
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Abstract

OBJECTIVE: Patients with type 1 diabetes now live long enough to experience cognitive decline. During middle age, they show mild cognitive deficits, but it is unknown whether severity increases with aging or whether cognitive profiles are similar to those of age-matched peers with and without diabetes. RESEARCH DESIGN AND METHODS: We tested and compared cognition in 82 individuals with 50 or more years of type 1 diabetes (Medalists), 31 age-matched individuals with type 2 diabetes, and 30 age-matched control subjects without diabetes. Medical histories and biospecimens were collected. We also evaluated the association of complications with cognition in Medalists only. RESULTS: Compared with control subjects, both individuals with type 1 diabetes and individuals with type 2 diabetes performed worse on immediate and delayed recall (P ≤ 0.002) and psychomotor speed in both hands (P ≤ 0.01) and showed a trend toward worse executive function (P = 0.05). In Medalists, cardiovascular disease was associated with decreased executive function and proliferative diabetic retinopathy with slower psychomotor speed. CONCLUSIONS: Both patients with type 1 and patients with type 2 diabetes showed overall worse cognition than control subjects. Further, in Medalists, a relationship between complications and cognition was seen. Although both groups with diabetes showed similar deficit patterns, the underlying mechanisms may be different. Now that patients with type 1 diabetes are living longer, efforts should be made to evaluate cognition and to identify modifying behaviors to slow decline.

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  • Older adults with type 1 diabetes mellitus have an increased risk of cognitive decline.

    “and have an increased risk of cognitive decline9”

    From The epidemiology of type 1 diabetes mellitus in older adults (2025) · cites this paper as [9]

    The Conclusions (page not supplied) report worse cognitive performance in older adults with long-duration type 1 diabetes than in age-matched controls. They also describe a longitudinal study in which cognitive decline relative to controls occurred among patients with significant comorbidities, but not among those without complications. The unqualified claim of increased risk of cognitive decline in older adults with type 1 diabetes is therefore broader than the evidence presented. (LLM, conf=0.85)

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Research works printed but not linked: 34

  1. [1]Krolewski AS. Epidemiology of late complications of diabetes. In Joslin's Diabetes Mellitus. 13th ed. Kahn CR, Weir GC, Eds. Philadelphia, PA, Lea & Febiger, 1994, p. 605–619 [Google Scholar]
  2. [2]Biessels GJ, Strachan MW, Visseren FL, Kappelle LJ, Whitmer RA. Dementia and cognitive decline in type 2 diabetes and prediabetic stages: towards targeted interventions. Lancet Diabetes Endocrinol 2014;2:246–255 [DOI] [PubMed] [Google Scholar]
  3. [3]Brands AM, Biessels GJ, de Haan EH, Kappelle LJ, Kessels RP. The effects of type 1 diabetes on cognitive performance: a meta-analysis. Diabetes Care 2005;28:726–735 [DOI] [PubMed] [Google Scholar]
  4. [4]Buckner RL. Memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron 2004;44:195–208 [DOI] [PubMed] [Google Scholar]
  5. [5]Elias MF, Beiser A, Wolf PA, Au R, White RF, D’Agostino RB. The preclinical phase of Alzheimer disease: a 22-year prospective study of the Framingham Cohort. Arch Neurol 2000;57:808–813 [DOI] [PubMed] [Google Scholar]
  6. [6]Schindler RJ. Dementia with cerebrovascular disease: the benefits of early treatment. Eur J Neurol 2005;12(Suppl. 3):17–21 [DOI] [PubMed] [Google Scholar]
  7. [8]Pambianco G, Costacou T, Ellis D, Becker DJ, Klein R, Orchard TJ. The 30-year natural history of type 1 diabetes complications: the Pittsburgh Epidemiology of Diabetes Complications Study experience. Diabetes 2006;55:1463–1469 [DOI] [PubMed] [Google Scholar]
  8. [9]Sun JK, Keenan HA, Cavallerano JD, et al. Protection from retinopathy and other complications in patients with type 1 diabetes of extreme duration: the Joslin 50-Year Medalist study. Diabetes Care 2011;34:968–974 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. [10]He ZH, D’Eon SA, Tinsley LJ, et al. Cardiovascular disease protection in long-duration type 1 diabetes and sex differences. Diabetes Care 2015;38:e73–e74 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. [11]Bergmann MM, Byers T, Freedman DS, Mokdad A. Validity of self-reported diagnoses leading to hospitalization: a comparison of self-reports with hospital records in a prospective study of American adults. Am J Epidemiol 1998;147:969–977 [DOI] [PubMed] [Google Scholar]
  11. [12]Martin LM, Leff M, Calonge N, Garrett C, Nelson DE. Validation of self-reported chronic conditions and health services in a managed care population. Am J Prev Med 2000;18:215–218 [DOI] [PubMed] [Google Scholar]
  12. [13]Okura Y, Urban LH, Mahoney DW, Jacobsen SJ, Rodeheffer RJ. Agreement between self-report questionnaires and medical record data was substantial for diabetes, hypertension, myocardial infarction and stroke but not for heart failure. J Clin Epidemiol 2004;57:1096–1103 [DOI] [PubMed] [Google Scholar]
  13. [14]Wechsler D. WASI Manual. San Antonio, TX, Psychological Corporation, 1999 [Google Scholar]
  14. [15]Strauss E, Sherman EMS, Spreen O. A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary. Oxford University Press, Oxford, U.K., 2006 [Google Scholar]
  15. [16]Biessels GJ, Reagan LP. Hippocampal insulin resistance and cognitive dysfunction. Nat Rev Neurosci 2015;16:660–671 [DOI] [PubMed] [Google Scholar]
  16. [17]Davis WA, Zilkens RR, Starkstein SE, Davis TM, Bruce DG. Dementia onset, incidence and risk in type 2 diabetes: a matched cohort study with the Fremantle Diabetes Study Phase I. Diabetologia 2017;60:89–97 [DOI] [PubMed] [Google Scholar]
  17. [18]Blázquez E, Velázquez E, Hurtado-Carneiro V, Ruiz-Albusac JM. Insulin in the brain: its pathophysiological implications for states related with central insulin resistance, type 2 diabetes and Alzheimer’s disease. Front Endocrinol (Lausanne) 2014;5:161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. [19]Popa-Wagner A, Buga AM, Popescu B, Muresanu D. Vascular cognitive impairment, dementia, aging and energy demand. A vicious cycle. J Neural Transm (Vienna) 2015;122(Suppl. 1):S47–S54 [DOI] [PubMed] [Google Scholar]
  19. [20]Brands AM, Kessels RP, Hoogma RP, et al. Cognitive performance, psychological well-being, and brain magnetic resonance imaging in older patients with type 1 diabetes. Diabetes 2006;55:1800–1806 [DOI] [PubMed] [Google Scholar]
  20. [21]Duinkerken Ev, Brands AM, van den Berg E, Henselmans JM, Hoogma RP, Biessels GJ; Utrecht Diabetic Encephalopathy Study Group . Cognition in older patients with type 1 diabetes mellitus: a longitudinal study. J Am Geriatr Soc 2011;59:563–565 [DOI] [PubMed] [Google Scholar]
  21. [22]Brands AM, Biessels GJ, Kappelle LJ, et al.; Utrecht Diabetic Encephalopathy Study Group . Cognitive functioning and brain MRI in patients with type 1 and type 2 diabetes mellitus: a comparative study. Dement Geriatr Cogn Disord 2007;23:343–350 [DOI] [PubMed] [Google Scholar]
  22. [23]Musen G, Lyoo IK, Sparks CR, et al. Effects of type 1 diabetes on gray matter density as measured by voxel-based morphometry. Diabetes 2006;55:326–333 [DOI] [PubMed] [Google Scholar]
  23. [24]Nelson AR, Sweeney MD, Sagare AP, Zlokovic BV. Neurovascular dysfunction and neurodegeneration in dementia and Alzheimer’s disease. Biochim Biophys Acta 2016;1862:887–900 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. [25]Tromp D, Dufour A, Lithfous S, Pebayle T, Despres O. Episodic memory in normal aging and Alzheimer disease: insights from imaging and behavioral studies. Ageing Res Rev 2015;24:232–262 [DOI] [PubMed] [Google Scholar]
  25. [26]Smolina K, Wotton CJ, Goldacre MJ. Risk of dementia in patients hospitalised with type 1 and type 2 diabetes in England, 1998-2011: a retrospective national record linkage cohort study. Diabetologia 2015;58:942–950 [DOI] [PubMed] [Google Scholar]
  26. [27]Trivedi MA, Murphy CM, Goetz C, et al. fMRI activation changes during successful episodic memory encoding and recognition in amnestic mild cognitive impairment relative to cognitively healthy older adults. Dement Geriatr Cogn Disord 2008;26:123–137 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. [28]Peña-Casanova J, Sánchez-Benavides G, de Sola S, Manero-Borrás RM, Casals-Coll M. Neuropsychology of Alzheimer’s disease. Arch Med Res 2012;43:686–693 [DOI] [PubMed] [Google Scholar]
  28. [29]Tan ZS, Beiser AS, Fox CS, et al. Association of metabolic dysregulation with volumetric brain magnetic resonance imaging and cognitive markers of subclinical brain aging in middle-aged adults: the Framingham Offspring Study. Diabetes Care 2011;34:1766–1770 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. [30]Nunley KA, Ryan CM, Aizenstein HJ, et al. Regional gray matter volumes as related to psychomotor slowing in adults with type 1 diabetes. Psychosom Med 2017;79:533–540 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. [31]Hernandez SL, Gong JH, Chen L, et al. Characterization of circulating and endothelial progenitor cells in patients with extreme-duration type 1 diabetes. Diabetes Care 2014;37:2193–2201 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. [32]Tinsley LJ, Kupelian V, D'Eon SA, Pober D, Sun JK, King GL, Keenan HA. Association of glycemic control with reduced risk of large vessel disease after more than 50 years of type 1 diabetes. J Clin Endocrinol Metabol 2017;102:3704–3711 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. [33]Bain SC, Gill GV, Dyer PH, et al. Characteristics of type 1 diabetes of over 50 years duration (the Golden Years Cohort). Diabet Med 2003;20:808–811 [DOI] [PubMed] [Google Scholar]
  33. [34]Weisman A, Lovblom LE, Keenan HA, et al. Diabetes care disparities in long-standing type 1 diabetes in Canada and the U.S.: a cross-sectional comparison. Diabetes Care 2018;41:88–95 [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. [35]Roberts RO, Cha RH, Mielke MM, et al. Risk and protective factors for cognitive impairment in persons aged 85 years and older. Neurology 2015;84:1854–1861 [DOI] [PMC free article] [PubMed] [Google Scholar]

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Authors
Musen, G., Tinsley, L. J., Marcinkowski, K. A., Pober, D., Sun, J. K., Khatri, M., Huynh, R., Lu, A., King, G. L., & Keenan, H. A.
Affiliations
  • Joslin Diabetes Center (US)
  • Eastern Virginia Medical School (US)
Corresponding author
Keenan, Hillary A.
ORCID
Venue
Diabetes Care
Publisher
American Diabetes Association
Published
2018-06-05
Volume
41
Issue
8
Pages
1749-1756
ISSN
  • 0149-5992 (ISSN-L)
  • 1935-5548
DOI
10.2337/dc17-1955
PMC
PMC6054500
OpenAlex
W2806961859
Cited by
65
References
1
Citations by year
2026: 4 · 2025: 7 · 2024: 12 · 2023: 7 · 2022: 12 · 2021: 10 · 2020: 7 · 2019: 4 · 2018: 1 · 2016: 1
FWCI
4.30
Type
journal article
Language
en
Open access
Licence
www.diabetesjournals.org/content/license (vor, 45 d)
Locations
  • Diabetes Care (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institute of Diabetes and Digestive and Kidney Diseases (P30-DK-036836, UL1-RR-025758-03, R24-DK-083957-01, DP3-DK-094333-01)
  • JDRF (17-2013-310)
Topics
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Education
Keywords
type 1 diabetes, cognitive decline, long-standing diabetes, type 2 diabetes, diabetes complications, cardiovascular disease, diabetic retinopathy, executive function, psychomotor speed, aging, cognitive function
MeSH terms
Adolescent, Adult, Aged, Cardiovascular Diseases, Child, Cognition, Cognition Disorders, Diabetes Mellitus, Type 1, Diabetes Mellitus, Type 2, Diabetic Angiopathies, Female, Humans, Male, Middle Aged, Time Factors, Case-Control Studies, Young Adult, Executive Function, Cognitive Dysfunction

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