Type 2 diabetes mellitus, cognitive impairment and dementia

Stewart, R.; Liolitsa, D.

doi:10.1046/j.1464-5491.1999.00027.x

Cited by 563Dementia and Cognitive Impairment ResearchDiabetes Treatment and ManagementNeurological Disease Mechanisms and Treatments

Type 2 diabetes mellitus, cognitive impairment and dementia

Stewart, R., Liolitsa, D.·1999·Diabetic Medicine

DOI 10.1046/j.1464-5491.1999.00027.x

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Abstract

Summary: Aims We set out to examine the evidence for an association between cognitive impairment or dementia and the presence of Type 2 diabetes mellitus (DM). We also sought evidence of potential mechanisms for such an association. Methods A literature search of three databases was performed and the reference lists of the papers so identified were examined, using English language papers only. Results We found evidence of cross‐sectional and prospective associations between Type 2 DM and cognitive impairment, probably both for memory and executive function. There is also evidence for an elevated risk of both vascular dementia and Alzheimer’s disease in Type 2 DM albeit with strong interaction of other factors such as hypertension, dyslipidaemia and apolipoprotein E phenotype. Both vascular and non‐vascular factors are likely to play a role in dementia in diabetes. Conclusions Current classification structures for dementia may not be adequate in diabetes, where mixed pathogenesis is likely. Further research into the mechanisms of cognitive impairment in Type 2 DM may allow us to challenge the concept of dementia, at least in these patients, as an irremediable disease. Diabet. Med. 16, 93–112 (1999)

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There is a growing literature indicating that individuals with diabetes have impairments in recent memory.
“There is a growing literature indicating that individuals with diabetes have impairments in recent memory (3–6).”
From Reduced glucose tolerance is associated with poor memory performance and hippocampal atrophy among normal elderly (2003) · cites this paper as [4]
Many of the studies suggesting diabetes is a risk factor for cognitive dysfunction were cross-sectional and unable to provide estimates of diabetes as a risk factor for future cognitive dysfunction.
“However, many of these studies were cross-sectional and were thus unable to provide estimates of diabetes as a risk factor for future cognitive dysfunction.”
From Cognitive decline and dementia in diabetes—systematic overview of prospective observational studies (2005) · cites this paper as [6]
Recent evidence from several epidemiological studies suggests that diabetes is a risk factor for cognitive dysfunction.
“Recent evidence from several epidemiological studies suggests that it is also a risk factor for cognitive dysfunction [3 -6].”
From Cognitive decline and dementia in diabetes—systematic overview of prospective observational studies (2005) · cites this paper as [6]
Only one of the review articles that summarised the available data on the relationship between diabetes and cognitive dysfunction provided a quantitative estimate.
“Indeed, only one [7] of the review articles that summarised the available data pertaining to this relationship [4, 6 -11] provided a quantitative estimate.”
From Cognitive decline and dementia in diabetes—systematic overview of prospective observational studies (2005) · cites this paper as [6]
Previous reviews of available longitudinal studies support the findings of this overview.
“These findings are supported by previous reviews of the available longitudinal studies [3, 4, 6].”
From Cognitive decline and dementia in diabetes—systematic overview of prospective observational studies (2005) · cites this paper as [6]

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Neuropsychological Function in Older Subjects with Non‐insulin‐dependent Diabetes Mellitus
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Cognition and depression in a cohort of aging men: Results from the Western Collaborative Group Study.
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Diabetes and Dementia: A Causal Association?
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Decreased cerebral blood perfusion in an NIDDM patient with an A-to-G mutation in the mitochondrial gene; a possible contribution to cognition deficits in diabetes mellitus
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Qualitative differences in the visual retention test performance of older non-insulin dependent diabetic patients
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Amyloid Plaque and Diabetes
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Complications of Diabetes in Childhood
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Detection of cerebrovascular disease in diabetic patients by means of the Kana test
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Flagged first, then by citations

Sorted by citations

Risk of dementia in diabetes mellitus: a systematic review
Biessels, G. J., Staekenborg, S., Brunner, E., Brayne, C., & Scheltens, P. (2006) · The Lancet Neurology · doi:10.1016/s1474-4422(05)70284-2 · Cited by 2,187 · see citing works
Brain insulin resistance in type 2 diabetes and Alzheimer disease: concepts and conundrums
Arnold, S. E., Arvanitakis, Z., Macauley-Rambach, S. L., Koenig, A. M., Wang, H.-Y., Ahima, R. S., Craft, S., Gandy, S., Buettner, C., Stoeckel, L. E., et al. (2018) · Nature Reviews Neurology · doi:10.1038/nrneurol.2017.185 · Cited by 1,597 · see citing works
Diabetes in Older Adults
Kirkman, M. S., Briscoe, V. J., Clark, N., Florez, H., Haas, L. B., Halter, J. B., Huang, E. S., Korytkowski, M. T., Munshi, M. N., Odegard, P. S., et al. (2012) · Diabetes Care · doi:10.2337/dc12-1801 · Cited by 1,274 · see citing works
Vascular Cognitive Impairment
O'Brien, J. T., Erkinjuntti, T., Reisberg, ‌., Román, G. C., Pantoni, L., Bowler, J., Ballard, C., DeCarli, C., Gorelick, P., Rockwood, K., et al. (2014) · International Journal of Stroke · doi:10.1111/ijs.12374_18 · Cited by 1,165 · see citing works
Vascular cognitive impairment
O'Brien, J. T., Erkinjuntti, T., Reisberg, B., Roman, G., Sawada, T., Pantoni, L., Bowler, J. V., Ballard, C., DeCarli, C., Gorelick, P. B., et al. (2003) · The Lancet Neurology · doi:10.1016/s1474-4422(03)00305-3 · Cited by 1,139 · see citing works
Cognitive decline and dementia in diabetes—systematic overview of prospective observational studies
Cukierman, T., Gerstein, H. C., & Williamson, J. D. (2005) · Diabetologia · doi:10.1007/s00125-005-0023-4 · Cited by 1,049 · see citing works
“These findings are supported by previous reviews of the available longitudinal studies [3, 4, 6].”
Midlife cardiovascular risk factors and risk of dementia in late life
Whitmer, R. A., Sidney, S., Selby, J., Johnston, S. C., & Yaffe, K. (2005) · Neurology · doi:10.1212/01.wnl.0000149519.47454.f2 · Cited by 1,238 · see citing works
Diabetes as a risk factor for dementia and mild cognitive impairment: a meta‐analysis of longitudinal studies
Cheng, G., Huang, C., Deng, H., & Wang, H. (2012) · Internal Medicine Journal · doi:10.1111/j.1445-5994.2012.02758.x · Cited by 1,040 · see citing works
Cognition and synaptic plasticity in diabetes mellitus
Gispen, W. H., & Biessels, G. J. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01656-8 · Cited by 772 · see citing works
Western diet consumption and cognitive impairment: Links to hippocampal dysfunction and obesity
Kanoski, S. E., & Davidson, T. L. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.12.003 · Cited by 674 · see citing works
“The most consistently reported cognitive deficits associated with insulin resistance and poor glycemic control in humans are found in memory tests that are also impaired in individuals with damage to the hippocampus, such as tests of delayed verbal memory [66,67].”
Background
Guidelines for improving the care of the older person with diabetes mellitus
California Healthcare Foundation/American Geriatrics Society, C. (2003) · Journal of the American Geriatrics Society · doi:10.1046/j.1532-5415.51.5s.1.x · Cited by 651 · see citing works
Cognition and diabetes: a lifespan perspective
Biessels, G. J., Deary, I. J., & Ryan, C. M. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(08)70021-8 · Cited by 646 · see citing works
Is Alzheimer’s disease a type 3 diabetes? A critical appraisal
Kandimalla, R., Thirumala, V., & Reddy, P. H. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2016.08.018 · Cited by 621 · see citing works
The relationship between impaired glucose tolerance, type 2 diabetes, and cognitive function
Awad, N., Gagnon, M., & Messier, C. (2004) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803390490514875 · Cited by 551 · see citing works
“There have been a number of excellent reviews describing and analyzing the impact of type 2 diabetes on cognitive functions (Biessels, van der Heide, Kamal, Bleys, & Gispen, 2002; Ryan, 1997; Stewart & Liolitsa, 1999; Strachan, Deary, Ewing, & Frier, 1997).”
BackgroundMethodInfluential
Insulin, insulin-degrading enzyme and amyloid-β peptide in Alzheimer's disease: review and hypothesis
Qiu, W. Q., & Folstein, M. F. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.01.004 · Cited by 538 · see citing works
Diabetes, impaired fasting glucose, and development of cognitive impairment in older women
Yaffe, K., Blackwell, T., Kanaya, A. M., Davidowitz, N., Barrett-Connor, E., & Krueger, K. (2004) · Neurology · doi:10.1212/01.wnl.0000134666.64593.ba · Cited by 520 · see citing works
Estrogen: A master regulator of bioenergetic systems in the brain and body
Rettberg, J. R., Yao, J., & Brinton, R. D. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.08.001 · Cited by 534 · see citing works
“Persons with diabetes have a high risk of cognitive dysfunction, including amnestic MCI (Luchsinger et al., 2007b; Solfrizzi et al., 2004) and all types of dementia (Brayne et al., 1998; Brismar et al., 2007; Northam et al., 2006; Ott et al., 1999; Ristow, 2004; Stewart and Liolitsa, 1999).”
Revisiting the cholinergic hypothesis in the development of Alzheimer's disease
Craig, L. A., Hong, N. S., & McDonald, R. J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.03.001 · Cited by 487 · see citing works
Brain Magnetic Resonance Imaging Correlates of Impaired Cognition in Patients With Type 2 Diabetes
Manschot, S., Brands, A. M. A., van der Grond, J., Kessels, R. P. C., Algra, A., Kappelle, L. J., Biessels, G. J., & on behalf of the Utrecht Diabetic Encephalopathy Study Group (2006) · Diabetes · doi:10.2337/diabetes.55.04.06.db05-1323 · Cited by 477 · see citing works
Ageing and diabetes: implications for brain function
Biessels, G. J., van der Heide, L. P., Kamal, A., Bleys, R. L. A. W., & Gispen, W. H. (2002) · European Journal of Pharmacology · doi:10.1016/s0014-2999(02)01486-3 · Cited by 458 · see citing works
Oxidative stress in Alzheimer disease
Gella, A., & Durany, N. (2009) · Cell Adhesion & Migration · doi:10.4161/cam.3.1.7402 · Cited by 459 · see citing works
What is the association between sedentary behaviour and cognitive function? A systematic review
Falck, R. S., Davis, J. C., & Liu-Ambrose, T. Y. L. (2016) · British Journal of Sports Medicine · doi:10.1136/bjsports-2015-095551 · Cited by 454 · see citing works
Fructose: a highly lipogenic nutrient implicated in insulin resistance, hepatic steatosis, and the metabolic syndrome
Dekker, M. J., Su, Q., Baker, C., Rutledge, A. C., & Adeli, K. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00283.2010 · Cited by 419 · see citing works
Diabetes mellitus and risk of dementia in the Kungsholmen project
Xu, W., Qiu, C., Wåhlin, Å., Winblad, B. G., & Fratiglioni, L. (2004) · Neurology · doi:10.1212/01.wnl.0000140291.86406.d1 · Cited by 409 · see citing works
(Pre)diabetes, brain aging, and cognition
Roriz‐Filho, J. S., Roriz, T. M. D. S., Rosset, I., Camozzato, A. L., dos Santos, A. C., Chaves, M. L. F., Moriguti, J. C., & Roriz‐Cruz, M. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.12.003 · Cited by 390 · see citing works
Risk factors for predicting progression from mild cognitive impairment to Alzheimer’s disease: a systematic review and meta-analysis of cohort studies
Li, J., Tan, L., Wang, H.-F., Tan, M., Tan, L., Xu, W., Zhao, Q., Wang, J., Jiang, T., & Yu, J. (2015) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2014-310095 · Cited by 360 · see citing works
Brain Imaging in Patients With Diabetes
van Harten, B., de Leeuw, F., Weinstein, H. C., Scheltens, P., & Biessels, G. J. (2006) · Diabetes Care · doi:10.2337/dc06-1637 · Cited by 349 · see citing works
Reduced glucose tolerance is associated with poor memory performance and hippocampal atrophy among normal elderly
Convit, A., Wolf, O. T., Tarshish, C., & de Leon, M. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0336073100 · Cited by 347 · see citing works
The relationship between type 2 diabetes and cognitive dysfunction: longitudinal studies and their methodological limitations
Allen, K. V., Frier, B. M., & Strachan, M. W. J. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.02.054 · Cited by 319 · see citing works
“Cross-sectional studies have suggested an association between type 2 diabetes, cognitive decline (particularly in aspects of verbal memory) and dementia (Strachan et al., 1997a; Stewart and Liolitsa, 1999) but a causal relationship can only be established through examination of the rate of change of cognitive function…”
Background
Hippocampal neuronal apoptosis in type 1 diabetes
Li, Z.-G., Zhang, W., Grunberger, G., & Sima, A. A. F. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02887-1 · Cited by 316 · see citing works
Apolipoprotein E, cholesterol metabolism, diabetes, and the convergence of risk factors for Alzheimer's disease and cardiovascular disease
Martins, I. J., Hone, E., Foster, J. K., Sünram-Lea, S. I., Gnjec, A., Fuller, S. J., Nolan, D., Gandy, S. E., & Martins, R. N. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001854 · Cited by 388 · see citing works
Changes in Cognitive Abilities Over a 4-Year Period Are Unfavorably Affected in Elderly Diabetic Subjects
Fontbonne, A., Berr, C., Ducimetière, P., & Alpérovitch, A. (2001) · Diabetes Care · doi:10.2337/diacare.24.2.366 · Cited by 297 · see citing works
The Role of Leptin and Adiponectin in Obesity-Associated Cognitive Decline and Alzheimer’s Disease
Forny‐Germano, L., Felice, F. G. D., & Vieira, M. N. N. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.01027 · Cited by 298 · see citing works
Insulin in the Brain: Sources, Localization and Functions
Ghasemi, R., Haeri, A., Dargahi, L., Mohamed, Z., & Ahmadiani, A. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8339-9 · Cited by 291 · see citing works
“The effect of diabetes mellitus on cognitive functions has also been reviewed in several other articles [139, 143].”
Background
Mid- and Late-Life Diabetes in Relation to the Risk of Dementia
Xu, W., Qiu, C., Gatz, M., Pedersen, N. L., Johansson, B., & Fratiglioni, L. (2009) · Diabetes · doi:10.2337/db08-0586 · Cited by 284 · see citing works
Diabetes mellitus and dementia
Pasquier, F., Boulogne, A., Leys, D., & Fontaine, P. (2006) · Diabetes & Metabolism · doi:10.1016/s1262-3636(07)70298-7 · Cited by 275 · see citing works
“Population studies show inconsistent results [8].”
BackgroundResultInfluential
Effect of the treatment of Type 2 diabetes mellitus on the development of cognitive impairment and dementia
Sastre, A. A., Vernooij, R. W. M., Harmand, M. G., & Martínez, G. (2017) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003804.pub2 · Cited by 271 · see citing works
Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats
Tuzcu, M., & Baydaş, G. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.03.024 · Cited by 272 · see citing works
Cognitive effects of insulin in the central nervous system
Park, C. R. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00016-1 · Cited by 270 · see citing works
Increased risk of Alzheimer's disease in Type II diabetes: insulin resistance of the brain or insulin-induced amyloid pathology?
Biessels, G. J., & Kappelle, L. J. (2005) · Biochemical Society Transactions · doi:10.1042/bst0331041 · Cited by 288 · see citing works
Change in Cognitive Function by Glucose Tolerance Status in Older Adults: A 4-Year Prospective Study of the Rancho Bernardo Study Cohort
Kanaya, A. M., Barrett-Connor, E., Gildengorin, G., & Yaffe, K. (2004) · Archives of Internal Medicine · doi:10.1001/archinte.164.12.1327 · Cited by 255 · see citing works
A 4 year follow-up study of cognitive functioning in patients with type 2 diabetes mellitus
on behalf of the Utrecht Diabetic Encephalopathy Study Group, van den Berg, E., Reijmer, Y. D., de Bresser, J., Kessels, R. P. C., Kappelle, L. J., & Biessels, G. J. (2009) · Diabetologia · doi:10.1007/s00125-009-1571-9 · Cited by 256 · see citing works
“These decrements are most consistently found in information-processing speed, verbal memory and executive functioning [6, 7], possibly reflecting a diminished ability to efficiently process unstructured information [8].”
Background
Comorbid type 2 diabetes mellitus and hypertension exacerbates cognitive decline: evidence from a longitudinal study
Hassing, L. B. (2004) · Age and Ageing · doi:10.1093/ageing/afh100 · Cited by 249 · see citing works
“Extensive research on the effects of diabetes on cognitive function in old age has provided mixed findings [4, 5].”
Background
Advanced BrainAGE in older adults with type 2 diabetes mellitus
Franke, K., Gaser, C., Manor, B., & Novak, V. (2013) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2013.00090 · Cited by 221 · see citing works
“Clinical manifestations of DM-related brain abnormalities include worse functional status (Stewart and Liolitsa, 1999; Biessels et al., 2006), deficits in cognition [i.e., verbal memory, mental flexibility, and processing speed (Gispen and Biessels, 2000; Cheng et al., 2012)], and depression…”
Background
Cognitive efficiency declines over time in adults with Type 1 diabetes: effects of micro- and macrovascular complications
Ryan, C. M., Geckle, M., & Orchard, T. J. (2003) · Diabetologia · doi:10.1007/s00125-003-1128-2 · Cited by 243 · see citing works
“A substantial body of literature has suggested that chronic hyperglycaemia and/or the occurrence of complications could directly or indirectly affect brain function [ 32 , 33].”
Background
Brain Insulin: Regulation, Mechanisms of Action and Functions
Gerozissis, K. (2003) · Cellular and Molecular Neurobiology · doi:10.1023/a:1022598900246 · Cited by 235 · see citing works
“In addition, an elevated risk for AD was observed in diabetic patients (Biessels et al., 2002; Gasparini et al., 2002; Stewart and Liolitsa, 1999).”
Background
Statins for the treatment of dementia
McGuinness, B., Craig, D., Bullock, R. A., Malouf, R. S., & Passmore, P. (2014) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd007514.pub3 · Cited by 232 · see citing works
Cerebral Hemodynamics and Vascular Risk Factors: Setting the Stage for Alzheimer's Disease
de la Torre, J. C. (2012) · Journal of Alzheimer's Disease · doi:10.3233/jad-2012-120793 · Cited by 219 · see citing works
“There is general agreement that DM2 in the elderly will increase the risk of cognitive impairment that often progresses to AD [122] but a controversy has risen whether this process is due to vascular changes in the brain or to the formation of A and tau phosphorylation.”
Background
Type 2 Diabetes and Cognitive Function in Community-Dwelling Elderly Women
Grodstein, F., Chen, J., Wilson, R. S., & Manson, J. E. (2001) · Diabetes Care · doi:10.2337/diacare.24.6.1060 · Cited by 223 · see citing works
Risk of Incident Alzheimer's Disease in Diabetic Patients: A Systematic Review of Prospective Trials
Kopf, D., & Frölich, L. (2009) · Journal of Alzheimer s Disease · doi:10.3233/jad-2009-1011 · Cited by 225 · see citing works
“Accordingly, a large number of studies, mainly of cross-sectional or case control design, have shown that diabetes is associated with cognitive impairment [4].”
Learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: interaction of diabetes and ageing
Kamal, A., Biessels, G. J., Duis, S., & Gispen, W. H. (2000) · Diabetologia · doi:10.1007/s001250051335 · Cited by 223 · see citing works
“Better understanding of this interaction may eventually challenge the concept of accelerated cognitive decline in elderly diabetic patients as an irremediable disorder [ 16 ].”
Background
Neuronal IGF‐1 resistance reduces Aβ accumulation and protects against premature death in a model of Alzheimer's disease
Freude, S., Hettich, M. M., Schumann, C., Stöhr, O., Koch, L., Köhler, C., Udelhoven, M., Leeser, U., Müller, M., Kubota, N., et al. (2009) · The FASEB Journal · doi:10.1096/fj.09-132043 · Cited by 218 · see citing works
Progression of brain atrophy and cognitive decline in diabetes mellitus
van Elderen, S. G. C., Roos, A., de Craen, A. J. M., Westendorp, R. G. J., Blauw, G. J., Jukema, J. W., Bollen, E. L. E. M., Middelkoop, H. A. M., van Buchem, M. A., & van der Grond, J. (2010) · Neurology · doi:10.1212/wnl.0b013e3181f25f06 · Cited by 207 · see citing works
Molecular links between Alzheimer’s disease and diabetes mellitus
Yang, Y., & Song, W. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.009 · Cited by 201 · see citing works
Metabolic and vascular determinants of impaired cognitive performance and abnormalities on brain magnetic resonance imaging in patients with type 2 diabetes
Manschot, S., Biessels, G. J., de Valk, H. W., Algra, A., Rutten, G. E. H. M., van der Grond, J., Kappelle, L. J., & on behalf of the Utrecht Diabetic Encephalopathy Study Group (2007) · Diabetologia · doi:10.1007/s00125-007-0792-z · Cited by 198 · see citing works
“Neuropsychological studies show that patients with type 2 diabetes mellitus have mild to moderate impairments in attention and executive functioning, information processing speed and memory (for reviews see [2, 3]).”
BackgroundInfluential
Neurotoxicity of Advanced Glycation End-Products for Cultured Cortical Neurons
Takeuchi, M., Bucala, R., Suzuki, T., Ohkubo, T., Yamazaki, M., Koike, T., Kameda, Y., & Makita, Z. (2000) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/59.12.1094 · Cited by 198 · see citing works
Type 2 diabetes and risk of cognitive impairment and dementia
Whitmer, R. A. (2007) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-007-0058-7 · Cited by 195 · see citing works
“A review article summarizing 19 studies found that in 13 of these studies, type 2 diabetes subjects had significantly lower scores on at least one cognitive test, and effects were especially strong for verbal memory and complex information processing [71, 72 ], suggesting a domain-specific effect of diabetes on cognit…”
Background
Statins for the prevention of dementia
McGuinness, B., Craig, D., Bullock, R., & Passmore, P. (2009) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003160.pub2 · Cited by 193 · see citing works
Peroxisome proliferator-activated receptor γ is expressed in hippocampal neurons and its activation prevents β-amyloid neurodegeneration: role of Wnt signaling
Inestrosa, N. C., Godoy, J. A., Quintanilla, R. A., KOENIG, C., & Bronfman, M. (2004) · Experimental Cell Research · doi:10.1016/j.yexcr.2004.09.032 · Cited by 187 · see citing works
Untitled work
(2000) · doi:10.1002/1520-7560(2000)9999:9999
Memory inhibition and energy regulation
Davidson, T. L., Kanoski, S. E., Walls, E. K., & Jarrard, L. E. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.09.004 · Cited by 183 · see citing works
“Type II diabetes, which involves insensitivity or resistance to the effects of circulating insulin, is also associated with cognitive deficits [99].”
Background
Hypothalamic-Pituitary-Adrenal Axis Dysregulation and Memory Impairments in Type 2 Diabetes
Bruehl, H., Rueger, M., Dziobek, I., Sweat, V., Tirsi, A., Javier, E., Arentoft, A., Wolf, O. T., & Convit, A. J. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-2540 · Cited by 184 · see citing works
Donepezil for vascular cognitive impairment
Malouf, R. S., & Birks, J. (2004) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd004395.pub2 · Cited by 182 · see citing works
Type 2 diabetes mellitus contributes to cognitive decline in old age: A longitudinal population-based study
Hassing, L. B., GRANT, M. D., Hofer, S. M., Pedersen, N. L., NILSSON, S. E., Berg, S., McClearn, G. E., & Johansson, B. E. A. (2004) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617704104165 · Cited by 182 · see citing works
“Even though there is a great number of studies that have examined neuropsychological function in relation to type 2 diabetes, the findings are mixed (for reviews, see Biessels, 1999; Ryan & Geckle, 2000; Stewart & Liolitsa, 1999; Strachan et al., 1997).”
Background
RETRACTED: Intranasal insulin prevents cognitive decline, cerebral atrophy and white matter changes in murine type I diabetic encephalopathy
Francis, G. J., Martinez, J. A., Liu, W. Q., Xu, K., Ayer, A. B., Fine, J. M., Tuor, U. I., Glazner, G. W., Hanson, L. R., Frey, W. H., et al. (2008) · Brain · doi:10.1093/brain/awn288 · Cited by 175 · see citing works
Retracted
Human cerebral neuropathology of Type 2 diabetes mellitus
Nelson, P. T., Smith, C. D., Abner, E. L., Schmitt, F. A., Scheff, S. W., Davis, G. J., Keller, J. N., Jicha, G. A., Davis, D. G., Wang, W., et al. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.08.005 · Cited by 177 · see citing works
“Almost one-half of the published population studies have been interpreted to show no effect of diabetes on cognition [17].”
Type 2 diabetes as a risk factor for cognitive impairment: current insights
Umegaki, H. (2014) · Clinical Interventions in Aging · doi:10.2147/cia.s48926 · Cited by 180 · see citing works
“Moreover, recent studies have indicated that older people with T2DM have a higher risk of cognitive dysfunction or dementia.(4) Ample evidence has indicated that T2DM is related not only to vascular dementia (VD) but also to the clinical diagnosis of Alzheimer’s disease (AD)-type dementia.”
Background
Diabetes Mellitus Is a Risk Factor for Vascular Dementia, but Not for Alzheimer’s Disease: A Population-Based Study of the Oldest Old
Hassing, L. B., Johansson, B. E. A., Nilsson, S. E., Berg, S., Pedersen, N. L., Gatz, M., & McClearn, G. E. (2002) · International Psychogeriatrics · doi:10.1017/s104161020200844x · Cited by 175 · see citing works
Role of apolipoprotein E in neurodegenerative diseases
Giau, V. V., Bagyinszky, E., An, S. S. A., & Kim, S. (2015) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s84266 · Cited by 170 · see citing works
“Recently, studies have showed that older patients with T2DM have a higher risk of cognitive dysfunction or dementia.(98) Moreover, T2DM was related not only to VD, but also to the clinical diagnosis of AD-type dementia.”
Background
Cognitive impairment and MRI correlates in the elderly patients with type 2 diabetes mellitus
van Harten, B., Oosterman, J. M., Muslimović, D., van Loon, B. J. P., Scheltens, P., & Weinstein, H. C. (2007) · Age and Ageing · doi:10.1093/ageing/afl180 · Cited by 171 · see citing works
“Results of the subjective memory questionnaire, global cognitive functioning tests, different cognitive domains and individual neuropsychological tests DM Control subjects P-value d . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .…”
BackgroundMethodInfluential
Change in Cognitive Performance From Midlife Into Old Age: Findings from the Midlife in the United States (MIDUS) Study
Hughes, M. L., Agrigoroaei, S., Jeon, M., Bruzzese, M., & Lachman, M. E. (2018) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617718000425 · Cited by 167 · see citing works
“…& D’Agostino, 2000; Karlamangla et al., 2005), sensory/motor functioning (Lindenberger & Baltes, 1994; Wingfield, Tun, & McCoy, 2005), diabetes (Stewart & Liolitsa, 1999; Wu et al., 2008; Yeung, Fischer, & Dixon, 2009), stress and allostatic load (Seeman, McEwen, Singer, Albert, & Rowe,…”
Cognition in the Early Stage of Type 2 Diabetes
Ruis, C., Biessels, G. J., Gorter, K. J., van den Donk, M., Kappelle, L. J., & Rutten, G. E. H. M. (2009) · Diabetes Care · doi:10.2337/dc08-2143 · Cited by 164 · see citing works
“Previous studies have shown decrements in memory function, executive function, and information-processing speed (4,5).”
Result
Effect of Intranasal Insulin on Cognitive Function: A Systematic Review
Shemesh, E., Rudich, A., Harman-Boehm, I., & Cukierman-Yaffe, T. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1802 · Cited by 162 · see citing works
Insulin resistance and pathological brain ageing
Cholerton, B., Baker, L. D., & Craft, S. (2011) · Diabetic Medicine · doi:10.1111/j.1464-5491.2011.03464.x · Cited by 160 · see citing works
Maintained exercise‐enhanced brain executive function related to cerebral lactate metabolism in men
Hashimoto, T., Tsukamoto, H., Takenaka, S., Olesen, N. D., Petersen, L. G., Sørensen, H., Nielsen, H. B., Secher, N. H., & Ogoh, S. (2018) · The FASEB Journal · doi:10.1096/fj.201700381rr · Cited by 156 · see citing works
A high fructose diet impairs spatial memory in male rats
Ross, A. P., Bartness, T. J., Mielke, J. G., & Parent, M. B. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.05.007 · Cited by 154 · see citing works
“For instance, extensive evidence suggests that peripheral insulin resistance and type 2 diabetes are associated with deficits in hippocampal-dependent declarative memory (Convit, 2005; Messier, 2005; Stewart and Liolitsa, 1999; Strachan, Deary, Ewing, and Frier, 1997; Zhao, Chen, Xu, Moore, Meiri, Quon, and Alkon, 199…”
Background
Guidelines for Improving the Care of the Older Person with Diabetes Mellitus
Ickowicz, E. (2003) · Cited by 152 · see citing works
Impairments in glucose tolerance can have a negative impact on cognitive function: A systematic research review
Lamport, D. J., Lawton, C. L., Mansfield, M. W., & Dye, L. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.10.008 · Cited by 150 · see citing works
“Several reviews have shown that type 2 diabetes is associated with cognitive impairments (Awad et al., 2004; Biessels et al., 2002; Stewart and Liolitsa, 1999; Strachan et al., 1997), and longitudinal research has shown that type 2 diabetes can result in accelerated cognitive decline (Allen et al.,…”
Cerebral dysfunction in type 1 diabetes: effects of insulin, vascular risk factors and blood-glucose levels
Brands, A. M. A., Kessels, R. P. C., de Haan, E. H. F., Kappelle, L. J., & Biessels, G. J. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.02.053 · Cited by 150 · see citing works
A four-day Western-style dietary intervention causes reductions in hippocampal-dependent learning and memory and interoceptive sensitivity
Attuquayefio, T., Stevenson, R. J., Oaten, M., & Francis, H. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172645 · Cited by 147 · see citing works
Cognitive impairment, physical disability and depressive symptoms in older diabetic patients: the Fremantle Cognition in Diabetes Study
Bruce, D. G., Casey, G. P., Grange, V., Clarnette, R. C., Almeida, O. P., Foster, J. K., Ives, F. J., & Davis, T. M. E. (2003) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(03)00084-6 · Cited by 145 · see citing works
Peripheral Hyperinsulinemia Promotes Tau Phosphorylation In Vivo
Freude, S., Plum, L., Schnitker, J., Leeser, U., Udelhoven, M., Krone, W., Brüning, J. C., & Schubert, M. (2005) · Diabetes · doi:10.2337/diabetes.54.12.3343 · Cited by 144 · see citing works
Risk of Hypoglycemia in Older Veterans with Dementia and Cognitive Impairment: Implications for Practice and Policy
Feil, D. G., Rajan, M., Soroka, O., Tseng, C., Miller, D. R., & POGACH, L. M. (2011) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2011.03726.x · Cited by 142 · see citing works
Self‐Reported Goals of Older Patients with Type 2 Diabetes Mellitus
Huang, E. S., Gorawara‐Bhat, R., & Chin, M. H. (2005) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2005.53119.x · Cited by 139 · see citing works
Antidiabetic drugs restore abnormal transport of amyloid-β across the blood–brain barrier and memory impairment in db/db mice
Chen, F., Dong, R. R., Zhong, K. L., Ghosh, A., Tang, S. S., Long, Y., Hu, M. Y., Miao, M. X., Liao, J. M., Sun, H. B., et al. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.07.023 · Cited by 137 · see citing works
Cognitive function and information processing in Type 2 diabetes
Cosway, R., Strachan, M. W. J., Dougall, A., Frier, B. M., & Deary, I. J. (2001) · Diabetic Medicine · doi:10.1046/j.1464-5491.2001.00577.x · Cited by 137 · see citing works
Brain Lesions on MRI in Elderly Patients with Type 2 Diabetes Mellitus
van Harten, B., Oosterman, J. M., van Loon, B. J. P., Scheltens, P., & Weinstein, H. C. (2006) · European Neurology · doi:10.1159/000098054 · Cited by 135 · see citing works
“Diabetes mellitus (DM) has been associated with cognitive impairment and dementia, particularly in the elderly [”
Background
Overweight and cognition
Nilsson, L., & Nilsson, E. D. (2009) · Scandinavian Journal of Psychology · doi:10.1111/j.1467-9450.2009.00777.x · Cited by 133 · see citing works
Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes
Alvarez, E. O., Beauquis, J., Revsin, Y., Banzán, A. M., Roig, P., Nicola, A. F. D., & Saravia, F. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.001 · Cited by 130 · see citing works
Statins for the prevention of dementia
McGuinness, B., Craig, D., Bullock, R., & Passmore, P. (2016) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003160.pub3 · Cited by 490 · see citing works
Vascular risk factors and Alzheimer’s disease
Cechetto, D. F., Hachinski, V., & Whitehead, S. N. (2008) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.8.5.743 · Cited by 129 · see citing works
Low BDNF is associated with cognitive deficits in patients with type 2 diabetes
Zhen, Y. F., Zhang, J., Liu, X. Y., Fang, H., Tian, L. B., Zhou, D. H., Kosten, T. R., & Zhang, X. Y. (2013) · Psychopharmacology · doi:10.1007/s00213-012-2942-3 · Cited by 126 · see citing works
“…performance in T2DM patients in our present study is concordant with most of the studies evaluating cognitive function in patients with T2DM (Stewart et al. 1999; Gold et al. 2007; Nooyens et al. 2010; Szémán et al. 2012), and with the higher risk that T2DM patients have for cognitive…”
Result
Hypercholesterolaemia and vascular dementia
Appleton, J. P., Scutt, P., Sprigg, N., & Bath, P. M. (2017) · Clinical Science · doi:10.1042/cs20160382 · Cited by 127 · see citing works
The impact of diabetes mellitus on cognitive decline in the oldest of the old: a prospective population-based study
van den Berg, E., de Craen, A. J. M., Biessels, G. J., Gussekloo, J., & Westendorp, R. G. J. (2006) · Diabetologia · doi:10.1007/s00125-006-0333-1 · Cited by 126 · see citing works
“While hypertension has been suggested to be an important determinant of impaired cognition in diabetes [ 4 ], in the present study no clear relationship was found between hypertension and cognitive function within the group of diabetes patients, in line with other recent studies [27, 29].”
Result
Reduced hippocampal neurogenesis and number of hilar neurones in streptozotocin‐induced diabetic mice: reversion by antidepressant treatment
Beauquis, J., Roig, P., Homo‐Delarche, F., Nicola, A. F. D., & Saravia, F. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04691.x · Cited by 128 · see citing works
“…performance in neuropsychological tests, impairments in learning and memory, high risk of dementia, Alzheimer’s disease and elevated incidence of depression (Flood et al., 1990; McCall, 1992; Biessels et al., 1994; Mankovsky, 1997; Helgason, 1998; Ott et al., 1999; Stewart & Liolitsa, 1999).”
Background
Glycogen synthase kinase-3 is increased in white cells early in Alzheimer's disease
Hye, A., Kerr, F., Archer, N. J., Foy, C., Poppe, M., Brown, R. G., Hamilton, G., Powell, J. F., Anderton, B. H., & Lovestone, S. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.10.031 · Cited by 125 · see citing works
Insulin-like growth factor I (IGF-I) and cognitive decline in older persons
Dik, M. G., Pluijm, S. M. F., Jonker, C., Deeg, D. J. H., Lomecky, M. Z., & Lips, P. T. A. M. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00136-7 · Cited by 124 · see citing works
Glycaemic Control for People with Type 2 Diabetes Mellitus in Bangladesh - An urgent need for optimization of management plan
Afroz, A., Ali, L., Karim, M. N., Alramadan, M. J., Alam, K., Magliano, D. J., & Billah, B. (2019) · Scientific Reports · doi:10.1038/s41598-019-46766-9 · Cited by 123 · see citing works
Exploring effects of type 2 diabetes on cognitive functioning in older adults.
Yeung, S. E., Fischer, A. L., & Dixon, R. A. (2009) · Neuropsychology · doi:10.1037/a0013849 · Cited by 121 · see citing works
“Third, selected measures of executive functioning have produced diabetes-related performance deficits in some (but not all) studies (Awad et al., 2004; Messier, 2005; Ryan & Geckle, 2000; Stewart & Liolitsa, 1999).”
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Authors: Stewart, R., & Liolitsa, D.
Corresponding author: Stewart, R.
ORCID: Stewart, R.
Venue: Diabetic Medicine
Publisher: Wiley
Published: 1999-02
Volume: 16
Issue: 2
Pages: 93-112
ISSN: 0742-3071 (ISSN-L)
1464-5491
DOI: 10.1046/j.1464-5491.1999.00027.x
OpenAlex: W2078868323
Cited by: 562
References: 145
Citations by year: 2026: 2 · 2025: 12 · 2024: 13 · 2023: 11 · 2022: 12 · 2021: 12 · 2020: 18 · 2019: 18 · 2018: 18 · 2017: 18 · 2016: 19 · 2015: 33 · 2014: 17 · 2013: 21 · 2012: 35
FWCI: 9.03
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 1057 d)
Locations: Diabetic Medicine (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Keywords: type 2 diabetes, cognitive impairment, dementia, vascular dementia, Alzheimer's disease, memory, executive function, hypertension, dyslipidemia, apolipoprotein E, dementia classification
MeSH terms: Cognition Disorders, Cross-Sectional Studies, Dementia, Diabetes Mellitus, Type 2, Humans, Population Surveillance, Prospective Studies, Risk Factors, Case-Control Studies

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Type 2 diabetes mellitus, cognitive impairment and dementia

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