Hostname: page-component-76fb5796d-zzh7m Total loading time: 0 Render date: 2024-04-28T07:47:14.943Z Has data issue: false hasContentIssue false

Clinical and Sociodemographic Factors Associated with Cognitive Impairment and Neuroprotection in Diabetes Patients

Published online by Cambridge University Press:  14 September 2015

Carlos Valiente-Barroso*
Affiliation:
Universidad Complutense (Spain)
Jesús Mª Alvarado-Izquierdo
Affiliation:
Universidad Complutense (Spain)
Emilio García García
Affiliation:
Universidad Complutense (Spain)
*
*Correspondence concerning this article should be addressed to Carlos Valiente Barroso. E-mail: carlosvbsiete@hotmail.com

Abstract

The aim of this study is to analyze the potential impact of factors (clinical and demographic variables and comorbidities) associated with Diabetes Mellitus (DM) on certain mental processes related to cognitive impairment, with special attention to the analysis of parameters that define processing speed and executive function. Neuropsychological examination of elderly Spanish patients (N = 59, 33 females, Mage 70.98 years) diagnosed with DM, in addition to application of an ad hoc questionnaire to collect information on comorbidities and other relevant demographic variables. Based on a cross-sectional design, correlational analysis was carried out. Cognitive performance showed an inverse relationship to age and cardiopathology while years of schooling and regular physical activity appeared as neuroprotective factors. DM is an illness which, linked to other variables, can be regarded as a risk factor for the development of cognitive impairment. Certain factors (physical activity and cognitive stimulation) have the potential to mitigate this tendency. There is a need to further our understanding of the neurobiological mechanisms involved.

Type
Research Article
Copyright
Copyright © Universidad Complutense de Madrid and Colegio Oficial de Psicólogos de Madrid 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acee, A. M. (2012). Type 2 diabetes and vascular dementia: Assessment and clinical strategies of care. Medsurg Nursing, 21, 349353.Google Scholar
Akisaki, T., Sakurai, T., Takata, T., Umegaki, H., Araki, A., Mizuno, S., … Ito, H. (2006). Cognitive dysfunction associates with white matter hyperintensities and subcortical atrophy on magnetic resonance imaging of the elderly diabetes mellitus Japanese elderly diabetes intervention trial (J-EDIT). Diabetes/Metabolism Research and Reviews, 22, 376384. http://dx.doi.org/10.1002/dmrr.632 Google Scholar
Allen, K. V., Frier, B. M., & Strachan, M. W. (2004). The relationship between type 2 diabetes and cognitive dysfunction: Longitudinal studies. European Journal of Pharmacology, 490, 169175.Google Scholar
Andel, R., Vigen, C., Mack, W. J., Clark, L. J., & Gatz, M. (2006). The effect of education and occupational complexity on rate of cognitive decline in alzheimer’s patients. Journal of the International Neuropsychological Society, 12, 147152.Google Scholar
Ardila, A., & Rosselli, M. (2007). Neuropsicología clínica [Clinical neuropsychology]. Mexico DF, Mexico: Manual Moderno.Google Scholar
Arvanitakis, Z., Wilson, R. S., Bienias, J. L., Evans, D. A., & Bennet, D. A. (2004). Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Archives of Neurology, 61, 661666. http://dx.doi.org/10.1001/archneur.61.5.661 Google Scholar
Baker, L. D., Frank, L. L., Foster-Schubert, K., Green, P. S., Wilkinson, C. W., McTiernan, A., … Craft, S. (2010). Aerobic exercise improves cognition for older adults with glucose intolerance, a risk factor for Alzheimer's disease. Journal of Alzheimer's Disease, 22, 569579. http://dx.doi.org/10.3233/JAD-2010-100768 Google Scholar
Beydoun, M. A., Beydoun, H. A., & Wang, Y. (2008). Obesity and central obesity as risk factors for incident dementia and its subtypes: A systematic review and meta-analysis. Obesity Reviews, 9, 204218. http://dx.doi.org/10.1111/j.1467-789X.2008.00473.x Google Scholar
Beisiegel, U., & Spector, A. A. (2001). Lipids and lipoproteins in the brain. Current Opinion in Lipidology, 12, 243244. http://dx.doi.org/10.1097/00041433-200106000-00001 Google Scholar
Biessels, G. J., Deary, I. J., & Ryan, C. M. (2008). Cognition and diabetes: A life-span perspective. The Lancet Neurology, 7, 184190. http://dx.doi.org/10.1016/S1474-4422(08)70021-8 CrossRefGoogle Scholar
Borroni, B., Premi, E., Bozzali, M., & Padovani, A. (2012). Reserve mechanisms in neurodegenerative diseases: From bench to bedside and back again. Current Medicinal Chemistry, 19, 61126118. http://dx.doi.org/10.2174/092986712804485737 Google Scholar
Bruce, D. G., Davis, W. A., Casey, G. P., Starkstein, S. E., Clarnette, R. M., Almeida, O. P., & Davis, T. M. E. (2008). Predictors of cognitive decline in older individuals with diabetes. Diabetes Care, 31, 21032107. http://dx.doi.org/10.2337/dc08-0562 Google Scholar
Bruehl, H., Rueger, M., Dziobek, I., Sweat, V., Tirsi, A., Javier, E., … Convit, A. (2007). Hypo-thalamic-pituitary-adrenal axis dysregulation and memory impairments in type 2 diabetes. The Journal of Clinical Endocrinology and Metabolism, 92, 24392445.Google Scholar
Cai, A., Li, L., Zhang, Y., Mo, Y., Mai, W., & Zhou, Y. (2013). Lipoprotein(a): A promising marker for residual cardiovascular risk assessment. Disease Markers, 35, 551559. http://dx.doi.org/10.1155/2013/563717 Google Scholar
Cukierman, T., Gerstein, H. C., &Williamson, J. D. (2005). Cognitive decline and dementia in diabetes-systematic overview of prospective studies. Diabetologia, 48, 24602469. http://dx.doi.org/10.1007/s00125-005-0023-4 Google Scholar
Cukierman-Yaffe, T. (2009). Relationship between baseline glycemic control and cognitive function in individuals with type 2 diabetes and other cardiovascular risk factors: The action to control cardiovascular risk in diabetes-memory in diabetes (ACCORD-MIND) trial. Diabetes Care, 32, e103. http://dx.doi.org/10.2337/dc09-0821 CrossRefGoogle ScholarPubMed
CIBERDEM. Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (2013). Estudio di@betes. [Diabetes Study]. Madrid, Spain: Centro de Investigación Biomédica en Red (CIBER) Instituto de Salud Carlos III. Retrieved from http://www.ciberdem.org/estudio_diabetes.php Google Scholar
Danaei, G., Finucane, M. M., Lu, Y., Singh, G. M., Cowan, M. J., Paciorek, C. J., … Ezzati, M. (2011). National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: Systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. The Lancet, 378, 3140. http://dx.doi.org/10.1016/S0140-6736(11)60679-X Google Scholar
Dasgupta, K., Khan, S., & Ross, N. A. (2010). Type 2 diabetes in Canada: Concentration of risk among most disadvantaged men but inverse social gradient across groups in women. Diabetic Medicine, 27, 522531. http://dx.doi.org/10.1111/j.1464-5491.2010.02982.x Google Scholar
De Melo, M., de Sa, E., & Gucciardi, E. (2013). Exploring differences in Canadian adult men and women with Diabetes management: Results from the Canadian community health survey. BMC Public Health, 13, 1089. http://dx.doi.org/10.1186/1471-2458-13-1089 Google Scholar
Diamond, A. (2002). Normal development of prefrontal cortex from birth to young adulyhood: Cognitive function, anatomy and biochemistry. In Stuss, D. T., & Knight, R. T. (Eds.). Principles of frontal lobes function. London, UK: Oxford University Press.Google Scholar
Folstein, M., Folstein, S. E., & McHugh, P. R. (1975). “Mini-Mental State” a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189198. http://dx.doi.org/10.1016/0022-3956(75)90026-6 Google Scholar
Foster, P. P., Rosenblatt, K. P., & Kuljiš, R. O. (2011). Exercise-induced cognitive plasticity, implications for mild cognitive impairment and Alzheimer's disease. Frontiers in Neurology, 2, 28. http://dx.doi.org/10.3389/fneur.2011.00028 CrossRefGoogle ScholarPubMed
Franco-Martín, M., Parra-Vidales, E., González-Palau, F., Bernate-Navarro, M., & Solis, A. (2013). Influencia del ejercicio físico en la prevención del deterioro cognitivo en las personas mayores: Revisión sistemática [The influence of physical exercise in the prevention of cognitive deterioration in the elderly:A systematic review]. Revista de Neurología, 56, 545554.CrossRefGoogle Scholar
Fratiglioni, L., & Wang, H. X. (2007). Brain reserve hypothesis in dementia. Journal of Alzheimer’s Disease, 12, 1122.Google Scholar
Freeman, L. R., Haley-Zitlin, V., Rosenberger, D. S., & Granholm, A. C. (2014). Damaging effects of a high-fat diet to the brain and cognition: A review of proposed mechanisms. Nutritional Neuroscience, 17, 241251. http://dx.doi.org/10.1179/1476830513Y.0000000092 CrossRefGoogle Scholar
Gazdzinski, S., Kornak, J., Weine, M. W., & Meyerhoff, D. J. (2008). Body mass index and magnetic resonance markers of brain integrity in adults. Annals of Neurology, 34, 20892096. http://dx.doi.org/10.1111/j.1530-0277.2010.01305.x Google Scholar
Gioia, G. A., Isquith, P. K., Guy, S. C., & Kenworthy, L. (2000). Behavior rating inventory of executive function. Neuropsychology, Development, and Cognition. Section C, Child Neuropsychology, 6, 235238.Google Scholar
Golden, J. C. (1994). Stroop. Test de colores y palabras [Stroop color–word Test]. Madrid, Spain: TEA.Google Scholar
Graham, N. L., Emery, T., & Hodges, J. R. (2005). Distinctive cognitive profile in Alzheimer’s diseases and subcortical vascular dementia. Journal of Neurology, Neurosurgery & Psychiatry, 75, 6171.Google Scholar
Gunstad, J., Paul, R. H., Cohen, R. A., Tate, D. F., Spitznagel, M. B., & Gordon, E. (2007). Elevated body mass index is associated with executive dysfunction in otherwise healthy adults. Comprehensive Psychiatry, 48, 5761. http://dx.doi.org/10.1016/j.comppsych.2006.05.001 Google Scholar
Haninen, T., Koivisto, K., Reinikainen, K. J., Vanhanen, M., Helkala, E. L., Soininen, H., … Riekkinen, P. J. (1996). Prevalence of age-associated cognitive decline in an elderly population. Age and Ageing, 25, 201205.CrossRefGoogle Scholar
Ho, N., Sommers, M. S., & Lucki, I. (2013). Effects of diabetes on hippocampal neurogenesis: Links to cognition and depression. Neuroscience & Biobehavioral Reviews, 37, 13461362. http://dx.doi.org/10.1016/j.neubiorev.2013.03.010 Google Scholar
Hughes, T. M., Lopez, O. L., Evans, R. W., Kamboh, M. I., Williamson, J. D., Klunk, W. E., … Kuller, L. H. (2014). Markers of cholesterol transport are associated with amyloid deposition in the brain. Neurobiology Aging, 35, 802807. http://dx.doi.org/10.1016/j.neurobiolaging.2013.09.040 Google Scholar
Jacobson, A. M., Musen, G., Ryan, C. M., Silvers, N., Cleary, P., Waberski, B., … Harth, J. (2007). Diabetes control and complications trial/epidemiology of diabetes interventions and complications study research group. Long-term effect of diabetes and its treatment on cognitive function. The New England Journal of Medicine, 356, 18421852.Google Scholar
Jarvik, G. P., Wijsman, E. M., Kukull, W. A., Schellenberg, G. D., Yu, C., & Larson, E. B. (1995). Interactions of apolipoprotein E genotype, total cholesterol level, age, and sex in prediction for Alzheimer’s disease: A case-control study. Neurobiology, 45, 10921096.Google Scholar
Jeong, S. K., Nam, H. S., Son, M. H., Son, E. J., & Cho, K. H. (2005). Interactive effect of obesity indexes on cognition. Dementia and Geriatric Cognitive Disorders, 19, 9196. http://dx.doi.org/10.1159/000082659 CrossRefGoogle ScholarPubMed
Joosten, H., van Eersel, M. E., Gansevoort, R. T., Bilo, H. J., Slaets, J. P., & Izaks, G. J. (2013). Cardiovascular risk profile and cognitive function in young, middle-aged, and elderly subjects. Stroke, 44, 15431549. http://dx.doi.org/10.1161/STROKEAHA.111.000496 Google Scholar
Kalmijn, S., Foley, D., White, L., Burchfiel, C. M., Curb, J. D., Peteovitch, H., … Launer, L. J. (2000). Metabolic cardiovascular syndrome and risk of dementia in Japanese American elderly men: The Honolulu Asia Aging Study. Arteriosclerosis, Thrombosis, and Vascular Biology, 20, 22552560. http://dx.doi.org/10.1161/01.ATV.20.10.2255 CrossRefGoogle ScholarPubMed
Katon, W. J., Lin, E. H., Williams, L. H., Ciechanowski, P., Heckbert, S. R., Ludman, E., … Von Korff, M. (2010). Comorbid depression is associated with an increased risk of dementia diagnosis in patients with diabetes: A prospective cohort study. Journal of General Internal Medicine, 25, 423429. http://dx.doi.org/10.1007/s11606-009-1248-6 Google Scholar
Knopman, D. S., Mosley, T. H., Catellier, D. J., & Sharrett, A. R. (2005). Atherosclerosis Risk in Communities (ARIC) Study. Cardiovascular risk factors and cerebral atrophy in a middle-aged cohort. Neurology, 65, 876881.Google Scholar
Lezak, M. D. (1982). The problem of assessing executive functions. International Journal of Psychology, 17, 281297. http://dx.doi.org/10.1080/00207598208247445 Google Scholar
Luria, A. R. (1969). Frontal lobe syndromes. In Vinken, P. J. & Bruyn, G. W.. (Eds.). Handbook of clinical neurology, (Vol. 2., pp. 725757). Amsterdam, the Netherlands: North Holland.Google Scholar
Manschot, S. M., Brands, A. M., van der Grond, J., Kessels, R. P., Algra, A., Kappelle, , … Biessels, G. J. (2006). Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes. Diabetes, 55, 11061113.Google Scholar
McFall, G. P., Wiebe, S. A., Vergote, D., Westaway, D., Jhamandas, J., & Dixon, R. A. (2013). IDE (rs6583817) polymorphism and type 2 diabetes differentially modify executive function in older adults. Neurobiology of Aging, 34, 22082216. http://dx.doi.org/10.1016/j.neurobiolaging.2013.03.010 Google Scholar
Mejía-Arango, S., & Zúñiga-Gil, C. (2011). Diabetes mellitus como factor de riesgo de demencia en la población adulta mayor mexicana [Diabetes Mellitus as a risk factor for dementia in the Mexican elder population]. Revista de Neurología, 53, 397405.Google Scholar
Nithianantharaiah, J., & Hannan, A. J. (2011). Mechanisms mediating brain and cognitive reserve: Experience- dependent neuroprotection and functional compensation in animal models of neurodegenerative diseases. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 35, 331339. http://dx.doi.org/10.1016/j.pnpbp.2010.10.026 Google Scholar
Obisesan, T. O. (2009). Hypertension and cognitive function. Clinics in Geriatric Medicine, 25, 259288. http://dx.doi.org/10.1016/j.cger.2009.03.002 Google Scholar
Obisesan, T. O., Obisesan, O. A., Martins, S., Alamgir, L., Bond, V., Maxwell, C, & Gillum, R. F. (2008). High blood pressure, hypertension, and high pulse pressure are associated with poorer cognitive function in persons aged 60 and older: The third national health and nutrition examination survey. Journal of the American Geriatrics Society, 56, 501509. http://dx.doi.org/10.1111/j.1532-5415.2007.01592.x Google Scholar
Ott, A., Stolk, R. P., van Harskamp, F., Po, H. A. P., Hofman, A., & Breteler, M. M. B. (1999). Diabetes mellitus and the risk of dementia. The Rotterdam Study. Neurology, 53, 19371942. http://dx.doi.org/10.1212/WNL.53.9.1937 Google Scholar
Pannacciulli, N., Del Parigi, A., Che, K., Le, D. S., Reiman, E. M., & Tataranni, P. A. (2006). Brain abnormalities in human obesity: A voxel-based morphometric study. Neuroimage, 31, 14191425. http://dx.doi.org/10.1016/j.neuroimage.2006.01.047 Google Scholar
Ravona-Springer, R., Luo, X., Schmeidler, J., Wysocki, M., Lesser, G. T., Rapp, M. A., … Beeri, M. S. (2011). The association of age with rate of cognitive decline in elderly individuals residing in supporting care facilities. Alzheimer Disease and Associated Disorders, 25, 312316. http://dx.doi.org/10.1097/WAD.0b013e31820d880e Google Scholar
Reitan, R. M., & Wolfson, D. (1985). The Halstead-Reitan neuropsychological test battery: Theory and clinical interpretation. Tucson, AZ: Neuropsychology Press.Google Scholar
Reitz, C., Tang, M. X., Manly, J., Mayeux, R., & Luchsinger, J. A. (2007). Hypertension and the risk of mild cognitive impairment. Archives of Neurology, 64, 17341740. http://dx.doi.org/10.1001/archneur.64.12.1734 Google Scholar
Rönnemaa, E., Zethelius, B., Sundelöf, J., Sundström, J., Degerman-Gunnarsson, M., Berne, C., … Kilander, L. (2008). Impaired insulin secretion increases the risk of Alzheimer disease. Neurology, 71, 10651071. http://dx.doi.org/10.1212/01.wnl.0000310646.32212.3a Google Scholar
Ryan, C. M., & Geckle, M. O. (2000). Circumscribed cognitive dysfunction in middle-aged adults with type 2 diabetes. Diabetes Care, 23, 14861493. http://dx.doi.org/10.2337/diacare.23.10.1486 Google Scholar
Sanz, C., Gautier, J. F., & Hanaire, H. (2010). Physical exercise for the prevention and treatment of type 2 diabetes. Diabetes & Metabolism, 36, 346351. http://dx.doi.org/10.1016/j.diabet.2010.06.001 Google Scholar
Shindo, A., Terada, S., Sato, S., Ikeda, C., Nagao, S., Oshima, E., … Uchitomi, Y. (2013). Trail making test part a and brain perfusion imaging in Mild Alzheimer’s Disease. Dementia and Geriatric Cognitive Disorders Extra, 3, 202211. http://dx.doi.org/10.1159/000350806 Google Scholar
Smith, P. J., Blumenthal, J. A., Hoffman, B. M., Cooper, H., Strauman, T. A., Welsh-Bohmer, K., … Sherwood, A. (2010). Aerobic exercise and neurocognitive performance: A meta-analytic review of randomized controlled trials. Psychosomatic Medicine, 72, 239252. http://dx.doi.org/10.1097/PSY.0b013e3181d14633 Google Scholar
Sommerfield, A. J., Deary, I. J., & Frier, B. M. (2004). Acute hyperglycemia alters mood state and impairs cognitive performance in people with type 2 diabetes. Diabetes Care, 27, 23352340. http://dx.doi.org/10.2337/diacare.27.10.2335 CrossRefGoogle ScholarPubMed
Soriguer, F., Goday, A., Bosch-Comas, A., Bordiú, E., Calle-Pascual, A., Carmena, R., … Vendrell, J. (2012). Prevalence of diabetes mellitus and impaired glucose regulation in Spain: TheDi@bet.esStudy. Diabetologia, 55(1), 8893. http://dx.doi.org/10.1007/s00125-011-2336-9 CrossRefGoogle Scholar
Spauwen, P. J. J., Köhler, S., Verhey, F. R. J., Stehouwer, C. D. A., & van Boxtel, M. P. J. (2013). Effects of type 2 diabetes on 12-year cognitive change: Results from the Maastricht aging study. Diabetes Care, 36, 15541561. http://dx.doi.org/10.2337/dc12-0746 Google Scholar
Subirats-Bayego, E., Subirats-Vila, G., & Soteras-Martínez, I. (2012). Prescripción del ejercicio físico: Indicaciones, posología y efectos adversos. [Exercise prescription: Indications, dosage and side effects]. Medicina Clínica, 138(1), 1824. http://dx.doi.org/10.1016/j.medcli.2010.12.008 Google Scholar
Toro, P., Degen, C., Pierer, M., Gustafson, D., Schröder, J., & Schönknecht, P. (2014). Cholesterol in mild cognitive impairment and Alzheimer's disease in a birth cohort over 14 years. European Archives of Psychiatry and Clinical Neurosciences, 264, 485492. http://dx.doi.org/10.1007/s00406-013-0468-2 Google Scholar
Trujillo, A. J., & Fleisher, L. K. (2013). Beyond income, access, and knowledge: Factors explaining the education gradient in prevention among older adults with diabetes and hypertension in Latin America. Journal of Aging and Health, 25, 13981424. http://dx.doi.org/10.1177/0898264313508190 Google Scholar
van den Berg, E., De Craen, A. J., Biessels, G. J., Gussekloo, J., & Westendorp, R. G. (2006). The impact of diabetes mellitus on cognitive decline in the oldest of the old: A prospective population-based study. Diabetologia, 49, 20152023.Google Scholar
van Harten, B., Oosterman, J., Muslimovic, D., van Loon, B. J., Scheltens, P., & Weinstein, H. C. (2007). Cognitive impairment and MRI correlates in the elderly patients with type 2 diabetes mellitus. Age Ageing, 36, 164170.Google Scholar
Ward, M. A., Carlsson, C. M., Trivedi, M. A., Sager, M. A., & Johnson, S. C. (2005). The effect of body mass index on global brain volume in middle-aged adults: A cross sectional study. BMC Neurology, 5, 23. http://dx.doi.org/10.1186/1471-2377-5-23 Google Scholar
Wechsler, D. (2008). WAIS IV. Escala de Inteligencia de Wechsler para Adultos IV. [Wechsler Adult Intelligence Scale]. Madrid, Spain: NCS Pearson, Inc.Google Scholar
West, R. L. (1996). An application of prefrontal cortex function theory to cognitive aging. Psychological Bulletin, 120, 272292. http://dx.doi.org/10.1037/0033-2909.120.2.272 Google Scholar
West, R. (2000). In defense of the frontal lobe hypothesis of cognitive aging. Journal of the International Neuropsychological Society, 6, 727729. http://dx.doi.org/10.1017/S1355617700666109 Google Scholar
Whitmer, R. A., Gustafson, D. R., Barrett-Connor, E., Haan, M. N., Gunderson, E. P., & Yaffe, K. (2008). Central obesity in midlife and risk of dementia three decades later. Neurology, 71, 10571064. http://dx.doi.org/10.1212/01.wnl.0000306313.89165.ef Google Scholar
Whitmer, R. A., Gunderson, E. P., Barrett-Connor, E., Quesenberry, C. P. Jr., & Yaffe, K. (2005). Obesity in middle age and future risk of dementia: A 27 year longitudinal population based study. British Medical Journal, 330, 1360. http://dx.doi.org/10.1136/bmj.38446.466238.E0 Google Scholar
Whitmer, R. A., Gunderson, E. P., Quesenberry, , Zhou, J., & Yaffe, K. (2007). Body mass index in midlife and risk of Alzheimer disease and vascular dementia. Current Alzheimer Research, 4, 103109. http://dx.doi.org/10.2174/156720507780362047 Google Scholar
World Health Organization (2010). Global status report on noncommunicable diseases. Geneva, Switzerland: Author. Retrieved fromhttp://www.who.int/nmh/publications/ncd_report2010/en/ Google Scholar
Wysocki, M., Luo, X., Schmeidler, J., Dahlman, K., Lesser, G. T., Grossman, , … Beeri, M. S. (2012). Hypertension is associated with cognitive decline in elderly people at high risk for dementia. American Journal of Geriatric Psychiatry, 20, 179187. http://dx.doi.org/10.1097/JGP.0b013e31820ee833 Google Scholar
Xia, W., Wang, S., Sun, Z., Bai, F., Zhou, Y., Yang, Y., … Yuan, Y. (2013). Altered baseline brain activity in type 2 diabetes: A resting-state fMRI study. Psychoneuroendocrinology, 38, 24932501. http://dx.doi.org/10.1016/j.psyneuen.2013.05.012 Google Scholar
Xu, W. L., Qiu, C. X., Wahlin, A., Winblad, B., & Fratiglioni, L. (2004). Diabetes mellitus and risk of dementia in the Kungsholmen project. A 6-year follow-up study. Neurology, 63, 11811186. http://dx.doi.org/10.1212/01.WNL.0000140291.86406.D1 Google Scholar