Type 1 diabetes‐associated cognitive decline: A meta‐analysis and update of the current literature 1型糖尿病相关的认知能力下降：一项对最新文献的meta分析

Tonoli, Cajsa; Heyman, Elsa; Roelands, Bart; Pattyn, Nathalie; Buyse, Luk; Piacentini, Maria Francesca; Berthoin, Serge; Meeusen, Romain

doi:10.1111/1753-0407.12193

Cited by 148Diabetes Management and ResearchDiabetes Management and EducationDiabetes and associated disorders

Type 1 diabetes‐associated cognitive decline: A meta‐analysis and update of the current literature 1型糖尿病相关的认知能力下降：一项对最新文献的meta分析

Tonoli, Cajsa, Heyman, Elsa, Roelands, Bart, Pattyn, Nathalie, Buyse, Luk, Piacentini, Maria Francesca, Berthoin, Serge, Meeusen, Romain·2014·Journal of Diabetes

DOI 10.1111/1753-0407.12193

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Abstract

Background: Type 1 diabetes (T1D) can have a significant impact on brain structure and function, which is referred to as T1D‐associated cognitive decline (T1DACD). Diabetes duration, early onset disease, and diabetes‐associated complications are all proposed as factors contributing to T1DACD. However, there have been no comparisons in T1DACD between children and adults with T1D. To obtain a better insight into the occurrence and effects of T1DACD in T1D, the aim of the present meta‐analysis was to investigate differences between children and adults and to analyse factors contributing T1DACD. Methods: Two electronic databases were consulted: PubMed and ISI W eb of K nowledge. Literature published up until the end of 2013 was included in the analysis. Effect sizes (C ohen's d), which are standardized differences between experimental and control groups, were calculated. Results: There was a small to modest decrease in cognitive performance in T1D patients compared with non‐diabetic controls. Children with T1D performed worse while testing for executive function, full intelligence quotient (IQ), and motor speed, whereas adults with T1D performed worse while testing the full, verbal and performance IQ, part of the executive function, memory, spatial memory, and motor speed. Episodes of severe hypoglycemia, chronic hyperglycemia, and age of onset can be significant factors influencing cognitive function in T1D. Conclusions: The findings in the literature suggest that T1DACD is more severe in adults than children, indicating that age and diabetes duration contribute to this T1DACD.

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Diabetes may cause acute and chronic neurocognitive changes, including cognitive decline affecting psychomotor speed, cognitive flexibility, attention, and visual perception.
“People with diabetes might also have both chronic and acute neurocognitive changes that include decline in cognitive function with detrimental effects on psychomotor speed, cognitive flexibility, attention, and visual perception.121,122”
From Type 1 diabetes (2018) · cites this paper as [122]

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Wright, R. J., Frier, B. M., & Deary, I. J. (2009) · Diabetes Care · doi:10.2337/dc09-0212 · Cited by 45 · see citing works
Gender differences in the learning status of diabetic children.
Holmes, C. S., Dunlap, W. P., Chen, R. S., et al. (1992) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.60.5.698 · Cited by 45 · see citing works
Effects of acute hypoglycaemia on auditory information processing in adults with Type I diabetes
Strachan, M. W. J., Ewing, F. M. E., Frier, B. M., McCrimmon, R. J., & Deary, I. J. (2003) · Diabetologia · doi:10.1007/s00125-002-0950-2 · Cited by 41 · see citing works
Cognitive function during insulin-induced hypoglycemia in humans: Short-term cerebral adaptation does not occur
Gold, A. E., MacLeod, K. M., Thomson, K. J., Frier, B. M., & Deary, I. J. (1995) · Psychopharmacology · doi:10.1007/bf02246299 · Cited by 40 · see citing works
Improvements in cognition, mood and behaviour following commencement of continuous subcutaneous insulin infusion therapy in children with type 1 diabetes mellitus: a pilot study
Knight, S., NORTHAM, E. A., Donath, S. M., Gardner, A., Harkin, N., Taplin, C. E., Joy, P., Cameron, F. J., & Ambler, G. R. (2008) · Diabetologia · doi:10.1007/s00125-008-1197-3 · Cited by 40 · see citing works
Cognitive function in adult offspring of women with Type 1 diabetes
Clausen, T. D., Mortensen, E. L., Schmidt, L., Mathiesen, E. R., Hansen, T. F., Jensen, D. M., Holm, S., Poulsen, L. K., From, M., & Damm, P. (2011) · Diabetic Medicine · doi:10.1111/j.1464-5491.2011.03300.x · Cited by 37 · see citing works
Decrease of vigilance assessed by EEG-mapping in Type I diabetic patients with history of recurrent severe hypoglycaemia
Howorka, K., Pumprla, J., Saletu, B., Anderer, P., Krieger, M., & Schabmann, A. (2000) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00041-4 · Cited by 36 · see citing works
Attentional functioning is impaired during acute hypoglycaemia in people with Type 1 diabetes
McAulay, V., Deary, I. J., Sommerfield, A., & Frier, B. M. (2005) · Diabetic Medicine · doi:10.1111/j.1464-5491.2005.01795.x · Cited by 36 · see citing works
Altered expression of histone and synaptic plasticity associated genes in the hippocampus of streptozotocin-induced diabetic mice
Thomas, J., Garg, M. L., & Smith, D. W. (2013) · Metabolic Brain Disease · doi:10.1007/s11011-013-9418-y · Cited by 30 · see citing works
Hypoglycaemia in childhood onset type 1 diabetes-part villain, but not the only one
NORTHAM, E. A., & Lin, A. P. (2009) · Pediatric Diabetes · doi:10.1111/j.1399-5448.2009.00545.x · Cited by 29 · see citing works
Effects of acute insulin-induced hypoglycaemia on psychomotor function: people with type 1 diabetes are less affected than non-diabetic adults
Geddes, J., Deary, I. J., & Frier, B. M. (2008) · Diabetologia · doi:10.1007/s00125-008-1112-y · Cited by 28 · see citing works
Rate of fall of blood glucose and physiological responses of counterregulatory hormones, clinical symptoms and cognitive function to hypoglycaemia in Type I diabetes mellitus in the postprandial state
Fanelli, C. G., Pampanelli, S., Porcellati, F., Bartocci, L., Scionti, L., Rossetti, P., & Bolli, G. B. (2003) · Diabetologia · doi:10.1007/s00125-002-0948-9 · Cited by 27 · see citing works
Effects of duration of diabetes on behavioural and cognitive parameters in streptozotocin-induced juvenile diabetic rats.
Rajashree, R., Kholkute, S. D., & Goudar, S. S. (2011) · PubMed · Cited by 24 · see citing works
Acute Hypoglycemia Impairs Nonverbal Intelligence
Warren, R. E., Allen, K. V., Sommerfield, A. J., Deary, I. J., & Frier, B. M. (2004) · Diabetes Care · doi:10.2337/diacare.27.6.1447 · Cited by 22 · see citing works
Absence of an Association Between Insulin-Dependent Diabetes Mellitus and Developmental Learning Difficulties
Crawford, S. G., Kaplan, B. J., & Field, L. L. (2004) · Hereditas · doi:10.1111/j.1601-5223.1995.00073.x · Cited by 18 · see citing works
Cognition and brain imaging in type 1 diabetes
Musen, G. (2008) · Current Diabetes Reports · doi:10.1007/s11892-008-0024-z · Cited by 17 · see citing works
Risk of adverse effects of intensified treatment in insulin-dependent diabetes mellitus: A meta-analysis
Egger, M., Davey Smith, G., Stettler, C., & Diem, P. (1997) · Diabetic Medicine · doi:10.1002/(sici)1096-9136(199711)14:11

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Type 1 diabetes
DiMeglio, L. A., Evans-Molina, C., & Oram, R. A. (2018) · The Lancet · doi:10.1016/s0140-6736(18)31320-5 · Cited by 1,561 · see citing works
Chronic peripheral inflammation, hippocampal neurogenesis, and behavior
Chesnokova, V., Pechnick, R. N., & Wawrowsky, K. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.01.017 · Cited by 299 · see citing works
ISPAD Clinical Practice Consensus Guidelines 2018: Psychological care of children and adolescents with type 1 diabetes
Delamater, A. M., de Wit, M., McDarby, V., Malik, J. A., Hilliard, M. E., Northam, E., & Acerini, C. L. (2018) · Pediatric Diabetes · doi:10.1111/pedi.12736 · Cited by 279 · see citing works
Effects of poverty on interacting biological systems underlying child development
Jensen, S. K. G., Berens, A. E., & Nelson, C. A. (2017) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(17)30024-x · Cited by 241 · see citing works
Psychological care of children and adolescents with type 1 diabetes
Delamater, A. M., de Wit, M., McDarby, V., Malik, J. A., & Acerini, C. L. (2014) · Pediatric Diabetes · doi:10.1111/pedi.12191 · Cited by 218 · see citing works
Impact of Early Diabetic Ketoacidosis on the Developing Brain
Aye, T., Mazaika, P. K., Mauras, N., Marzelli, M. J., Shen, H., Hershey, T., Cato, A., Weinzimer, S. A., White, N. H., Tsalikian, E., et al. (2019) · Diabetes Care · doi:10.2337/dc18-1405 · Cited by 124 · see citing works
Neurocognitive consequences of diabetes.
Ryan, C. M., van Duinkerken, E., & Rosano, C. (2016) · American Psychologist · doi:10.1037/a0040455 · Cited by 136 · see citing works
The effect of type 1 diabetes on the developing brain
Cameron, F. J., NORTHAM, E. A., & Ryan, C. M. (2019) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(19)30055-0 · Cited by 106 · see citing works
Defining Pathways for Development of Disease-Modifying Therapies in Children With Type 1 Diabetes: A Consensus Report
Wherrett, D. K., Chiang, J. L., Delamater, A. M., DiMeglio, L. A., Gitelman, S. E., Gottlieb, P. A., Herold, K. C., Lovell, D. J., Orchard, T. J., Ryan, C. M., et al. (2015) · Diabetes Care · doi:10.2337/dc15-1429 · Cited by 94 · see citing works
Diabetes mellitus in the young and the old: Effects on cognitive functioning across the life span
van Duinkerken, E., & Ryan, C. M. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104608 · Cited by 83 · see citing works
Clinically significant cognitive impairment in older adults with type 1 diabetes
Chaytor, N. S., Barbosa-Leiker, C., Ryan, C. M., Germine, L. T., Hirsch, I. B., & Weinstock, R. S. (2019) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2018.04.003 · Cited by 87 · see citing works
Diabetes, antidiabetic medications and risk of dementia: A systematic umbrella review and meta‐analysis
Defo, A. K., Bakula, V., Pisaturo, A., Labos, C., Wing, S. S., & Daskalopoulou, S. S. (2023) · Diabetes Obesity and Metabolism · doi:10.1111/dom.15331 · Cited by 75 · see citing works
Continuous subcutaneous insulin infusion versus multiple daily injection regimens in children and young people at diagnosis of type 1 diabetes: pragmatic randomised controlled trial and economic evaluation
Blair, J., McKay, A., Ridyard, C. H., Thornborough, K., Bedson, E., Peak, M., Didi, M., Annan, F., Gregory, J. W., Hughes, D. A., et al. (2019) · BMJ · doi:10.1136/bmj.l1226 · Cited by 73 · see citing works
A Systematic Review and Meta-analysis of Executive Function Performance in Type 1 Diabetes Mellitus
Broadley, M. M., White, M. J., & Andrew, B. (2017) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000460 · Cited by 70 · see citing works
Ellagic acid protects against diabetes-associated behavioral deficits in rats: Possible involved mechanisms
Farbood, Y., Rashno, M., Ghaderi, S., Khoshnam, S. E., Sarkaki, A., Rashidi, K., Rashno, M. M., & Badavi, M. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.03.078 · Cited by 66 · see citing works
Glycemic extremes are related to cognitive dysfunction in children with type 1 diabetes: A meta‐analysis
He, J., Ryder, A. G., Li, S., Liu, W., & Zhu, X. (2018) · Journal of Diabetes Investigation · doi:10.1111/jdi.12840 · Cited by 69 · see citing works
Type 1 diabetes-associated cognitive impairment and diabetic peripheral neuropathy in Chinese adults: results from a prospective cross-sectional study
Ding, X., Fang, C., Li, X., Cao, Y., Zhang, Q., Huang, Y., Pan, J., & Zhang, X. (2019) · BMC Endocrine Disorders · doi:10.1186/s12902-019-0359-2 · Cited by 60 · see citing works
A longitudinal investigation of cognitive function in children and adolescents with type 1 diabetes mellitus
Kirchhoff, B. A., Jundt, D. K., Doty, T., & Hershey, T. G. (2016) · Pediatric Diabetes · doi:10.1111/pedi.12414 · Cited by 59 · see citing works
Construct validity, ecological validity and acceptance of self-administered online neuropsychological assessment in adults
Chaytor, N. S., Barbosa‐Leiker, C., Germine, L. T., Fonseca, L. M., McPherson, S., & Tuttle, K. R. (2020) · The Clinical Neuropsychologist · doi:10.1080/13854046.2020.1811893 · Cited by 57 · see citing works
Prevalence of dental caries in children and adolescents with type 1 diabetes: a systematic review and meta-analysis
Wang, Y., Xing, L., Yu, H., & Zhao, L. (2019) · BMC Oral Health · doi:10.1186/s12903-019-0903-5 · Cited by 57 · see citing works
Preventive effects of Salvia officinalis L. against learning and memory deficit induced by diabetes in rats: Possible hypoglycaemic and antioxidant mechanisms
Hasanein, P., Felehgari, Z., & Emamjomeh, A. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.04.045 · Cited by 55 · see citing works
Neurotrophins and cognitive functions in T1D compared with healthy controls: effects of a high-intensity exercise
Tonoli, C., Heyman, E., Buyse, L., Roelands, B., Piacentini, M. F., Bailey, S. P., Pattyn, N., Berthoin, S., & MEEUSEN, R. R. (2014) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2014-0098 · Cited by 46 · see citing works
Self-citation
Naringin ameliorates cognitive deficits via oxidative stress, proinflammatory factors and the PPARγ signaling pathway in a type 2 diabetic rat model
QI, Z., Xu, Y., Liang, Z., Li, S., WANG, J., WEI, Y., & Dong, B. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.4232 · Cited by 44 · see citing works
Functional magnetic resonance imaging reveals differences in brain activation in response to thermal stimuli in diabetic patients with and without diabetic peripheral neuropathy
Li, J., Zhang, W., Wang, X., Yuan, T., Liu, P., Wang, T., Shen, L., Huang, Y., Li, N., You, H., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0190699 · Cited by 43 · see citing works
Altered Brain Dynamics in Patients With Type 1 Diabetes During Working Memory Processing
Embury, C. M., Wiesman, A. I., Proskovec, A. L., Heinrichs‐Graham, E., McDermott, T. J., Lord, G. H., Brau, K. L., Drincic, A., Desouza, C. V., & Wilson, T. W. (2018) · Diabetes · doi:10.2337/db17-1382 · Cited by 40 · see citing works
Type 1 Diabetes in Parents and Risk of Attention Deficit/Hyperactivity Disorder in Offspring: A Population-Based Study in Sweden
Ji, J., Chen, T., Sundquist, J., & Sundquist, K. (2018) · Diabetes Care · doi:10.2337/dc17-0592 · Cited by 38 · see citing works
Continuous subcutaneous insulin infusion versus multiple daily injections in children and young people at diagnosis of type 1 diabetes: the SCIPI RCT
Blair, J., McKay, A., Ridyard, C. H., Thornborough, K., Bedson, E., Peak, M., Didi, M., Annan, F., Gregory, J. W., Hughes, D. A., et al. (2018) · Health Technology Assessment · doi:10.3310/hta22420 · Cited by 39 · see citing works
Patient and Healthcare Professionals Perspectives on the Delivery of Exercise Education for Patients With Type 1 Diabetes
Litchfield, I. J., Andrews, R. C., Narendran, P., & Greenfield, S. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00076 · Cited by 37 · see citing works
Plant-Derived Bioactive Compounds: Exploring Neuroprotective, Metabolic, and Hepatoprotective Effects for Health Promotion and Disease Prevention
Direito, R., Barbalho, S. M., Sepodes, B. M. N., & Figueira, M. E. (2024) · Pharmaceutics · doi:10.3390/pharmaceutics16050577 · Cited by 39 · see citing works
Physical exercise reverses spatial memory deficit and induces hippocampal astrocyte plasticity in diabetic rats
de Senna, P. N., Bagatini, P. B., Galland, F., Bobermin, L. D., do Nascimento, P. S., Nardin, P., Tramontina, A. C., Gonçalves, C. A., Achaval, M., & Xavier, L. L. (2016) · Brain Research · doi:10.1016/j.brainres.2016.10.024 · Cited by 35 · see citing works
Investigating the effects ofCitrullus colocynthison cognitive performance and anxiety-like behaviors in STZ-induced diabetic rats
Rajizadeh, M. A., Aminizadeh, A. H., Esmaeilpour, K., Bejeshk, M. A., Sadeghi, A., & Salimi, F. (2021) · International Journal of Neuroscience · doi:10.1080/00207454.2021.1916743 · Cited by 31 · see citing works
Cognitive deficits associated with impaired awareness of hypoglycaemia in type 1 diabetes
Hansen, T. I., Olsen, S. E., Haferstrom, E. C. D., Sand, T., Frier, B. M., Haberg, A. K., & Bjørgaas, M. R. (2017) · Diabetologia · doi:10.1007/s00125-017-4233-3 · Cited by 30 · see citing works
The role of traditional Chinese medicine in the treatment of cognitive dysfunction in type 2 diabetes
Meng, J., Zhu, Y., Ma, H., Wang, X., & Zhao, Q. (2021) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2021.114464 · Cited by 29 · see citing works
Altered Integration of Structural Covariance Networks in Young Children With Type 1 Diabetes
Hosseini, S. M. H., Mazaika, P. K., Mauras, N., Buckingham, B. A., WEINZIMER, S. A., Tsalikian, E., White, N. H., & Reiss, A. L. (2016) · Human Brain Mapping · doi:10.1002/hbm.23293 · Cited by 27 · see citing works
Patients with type 1 diabetes in Sweden experience more fatigue than the general population
Segerstedt, J., Lundqvist, R., & Eliasson, M. (2015) · Journal of Clinical & Translational Endocrinology · doi:10.1016/j.jcte.2015.06.001 · Cited by 26 · see citing works
Corresponding risk factors between cognitive impairment and type 1 diabetes mellitus: A narrative review
Jin, C.-Y., Yu, S., Yin, J.-T., Yuan, X.-Y., & Wang, X. (2022) · Heliyon · doi:10.1016/j.heliyon.2022.e10073 · Cited by 26 · see citing works
Short and long term neuro-behavioral alterations in type 1 diabetes mellitus pediatric population
Litmanovitch, E. (2015) · World Journal of Diabetes · doi:10.4239/wjd.v6.i2.259 · Cited by 26 · see citing works
Simvastatin ameliorates memory impairment and neurotoxicity in streptozotocin-induced diabetic mice
Fang, S., Xie, H., Fang, C., Hu, M. Y., Long, Y., Sun, H., Kong, L., Hong, H., & Tang, S. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.05.001 · Cited by 26 · see citing works
Incidence and Risk Profile of Dementia in the Regions of Middle East and North Africa
Bhalla, D., Lotfalinezhad, E., Amini, F., Salmannejad, M., Nezhad, V. R. B., Kooshalshah, S. F. R., Delbari, A., Fadayevatan, R., Irmansyah, I., Abdelrahman, A., et al. (2018) · Neuroepidemiology · doi:10.1159/000487761 · Cited by 24 · see citing works
Influence of Chronic Coenzyme Q10 Supplementation on Cognitive Function, Learning, and Memory in Healthy and Diabetic Middle-Aged Rats
Monsef, A., Shahidi, ‬., & Komaki‬, A. (2018) · Neuropsychobiology · doi:10.1159/000495520 · Cited by 23 · see citing works
The effect of acute cocoa flavanol intake on the BOLD response and cognitive function in type 1 diabetes: a randomized, placebo-controlled, double-blinded cross-over pilot study
Decroix, L., Schuerbeek, P. V., Tonoli, C., Cutsem, J. V., Soares, D. D., Heyman, E., Vanderhasselt, T., Verrelst, R., Raeymaekers, H., Mey, J. D., et al. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05306-z · Cited by 23 · see citing works
Self-citation
Sesamin alleviates diabetes-associated behavioral deficits in rats: The role of inflammatory and neurotrophic factors
Ghaderi, S., Rashno, M., Nesari, A., Khoshnam, S. E., Sarkaki, A., Khorsandi, L., Farbood, Y., & Rashidi, K. (2021) · International Immunopharmacology · doi:10.1016/j.intimp.2020.107356 · Cited by 23 · see citing works
Cognitive functions in children and adolescents with early-onset diabetes mellitus in Egypt
El-Asrar, M. A., Andrawes, N. G., Rabie, M., El‐Gabry, D. A., Khalifa, A., El-Sherif, M., & Aziz, K. A. (2016) · Applied Neuropsychology Child · doi:10.1080/21622965.2016.1224186 · Cited by 22 · see citing works
The Role of School Nurse Presence in Parent and Student Perceptions of Helpfulness, Safety, and Satisfaction With Type 1 Diabetes Care
Wilt, L. (2020) · The Journal of School Nursing · doi:10.1177/1059840520918310 · Cited by 21 · see citing works
Brain functions and cognition on transient insulin deprivation in type 1 diabetes
Creo, A. L., CORTES, T. M., Jo, H. J., Huebner, A. R., Dasari, S., Tillema, J., Lteif, A. N., Klaus, K. A., Ruegsegger, G. N., Kudva, Y. C., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.144014 · Cited by 21 · see citing works
Cognitive function in individuals with and without painful and painless diabetic polyneuropathy—A cross‐sectional study in type 1 diabetes
Croosu, S. S., Gjela, M., Røikjer, J., Hansen, T. M., Mørch, C. D., Frøkjær, J. B., & Ejskjær, N. (2023) · Endocrinology Diabetes & Metabolism · doi:10.1002/edm2.420 · Cited by 20 · see citing works
Brain Activation and Psychomotor Speed in Middle-Aged Patients with Type 1 Diabetes: Relationships with Hyperglycemia and Brain Small Vessel Disease
Hwang, M., Tudorascu, D., Nunley, K. A., Karim, H. T., Aizenstein, H. J., Orchard, T. J., & Rosano, C. (2016) · Journal of Diabetes Research · doi:10.1155/2016/9571464 · Cited by 21 · see citing works
A systematic review of the effect of prior hypoglycaemia on cognitive function in type 1 diabetes
CHANDRAN, S. R., Jacob, P., & Choudhary, P. (2020) · Therapeutic Advances in Endocrinology and Metabolism · doi:10.1177/2042018820906017 · Cited by 22 · see citing works
Lower cognitive performance among long-term type 1 diabetes survivors
Awad, A., Lundqvist, R., Rolandsson, O., Sundström, A. E., & Eliasson, M. (2017) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2017.04.023 · Cited by 19 · see citing works
Effect of verbal task complexity in a working memory paradigm in patients with type 1 diabetes. A fMRI study
Guàrdia‐Olmos, J., Gallardo‐Moreno, G. B., Gudayol‐Ferré, E., Peró, M., & González‐Garrido, A. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0178172 · Cited by 19 · see citing works
Regional Cerebral Hemodynamic Response to Incremental Exercise Is Blunted in Poorly Controlled Patients With Uncomplicated Type 1 Diabetes
Tagougui, S., Fontaine, P., Leclair, E., Aucouturier, J., Matran, R., Oussaidene, K., Descatoire, A., Prieur, F., Mucci, P., Vambergue, A., et al. (2015) · Diabetes Care · doi:10.2337/dc14-1792 · Cited by 18 · see citing works
Self-citation
Resting-state functional MR imaging shed insights into the brain of diabetes
Wang, Y. F., Ji, X. M., Lu, G., & Zhang, L. J. (2016) · Metabolic Brain Disease · doi:10.1007/s11011-016-9872-4 · Cited by 18 · see citing works
Depressed mitochondrial function and electron transport Complex II-mediated H 2 O 2 production in the cortex of type 1 diabetic rodents
Chowdhury, S. R., Djordjevic, J., Thomson, E. A., Smith, D. R., Albensi, B. C., & Fernyhough, P. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.05.006 · Cited by 18 · see citing works
Structural Gray and White Matter Differences in Patients With Type 1 Diabetes and Impaired Awareness of Hypoglycemia
Stantonyonge, N., Sampedro, F., Méndez, J., Martínez‐Horta, S., Chico, A. I., & Gómez‐Ansón, B. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa832 · Cited by 16 · see citing works
A SLC20A2 gene mutation carrier displaying ataxia and increased levels of cerebrospinal fluid phosphate
Paucar, M., Almqvist, H., Jelić, V., Hagman, G., Jörneskog, G., Holmin, S., Björkhem, I., & Svenningsson, P. (2017) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2017.02.007 · Cited by 17 · see citing works
Cognition in Adults and Older Adults With Type 1 Diabetes: Chicken or Egg?
Chaytor, N. S. (2016) · Diabetes Spectrum · doi:10.2337/ds16-0050 · Cited by 15 · see citing works
Markers for cognitive impairments and variability of glycaemia in patients with type 1 diabetes mellitus
Самойлова, Ю. Г., Rotkank, M. A., Жукова, Н. Г., Матвеева, М. В., Tolmachev, I. V., & Kudlay, D. A. (2018) · S S Korsakov Journal of Neurology and Psychiatry · doi:10.17116/jnevro20181184148-51 · Cited by 15 · see citing works
Impaired cognitive processing speed in type 1 diabetic patients who had severe/recurrent hypoglycaemia
Bortolotti, S., Zarantonello, L., Uliana, A., Vitturi, N., Schiff, S., Bisiacchi, P. S., Avogaro, A., Amodio, P., & Maran, A. (2018) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2018.08.005 · Cited by 15 · see citing works
Regional Gray Matter Volumes as Related to Psychomotor Slowing in Adults with Type 1 Diabetes
Nunley, K. A., Ryan, C. M., Aizenstein, H. J., Jennings, J. R., MacCloud, R. L., Orchard, T. J., & Rosano, C. (2017) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000449 · Cited by 16 · see citing works
The impact of type 1 diabetes on neural activity serving attention
Embury, C. M., Wiesman, A. I., McDermott, T. J., Proskovec, A. L., Heinrichs‐Graham, E., Lord, G. H., Brau, K. L., Drincic, A., Desouza, C. V., & Wilson, T. W. (2018) · Human Brain Mapping · doi:10.1002/hbm.24431 · Cited by 14 · see citing works
Biochemical mechanism underlying the pathogenesis of diabetic retinopathy and other diabetic complications in humans: the methanol-formaldehyde-formic acid hypothesis
Zhu, B. T. (2022) · Acta Biochimica et Biophysica Sinica · doi:10.3724/abbs.2022012 · Cited by 13 · see citing works
The Relationships Among School Nurse to Student Ratios, Self-Efficacy, and Glycemic Control in Adolescents With Type 1 Diabetes
Wilt, L. (2019) · The Journal of School Nursing · doi:10.1177/1059840519870314 · Cited by 13 · see citing works
Altered motor dynamics in type 1 diabetes modulate behavioral performance
Embury, C. M., Heinrichs‐Graham, E., Lord, G. H., Drincic, A., Desouza, C. V., & Wilson, T. W. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.101977 · Cited by 12 · see citing works
Functional near‐infrared spectroscopy detects increased activation of the brain frontal‐parietal network in youth with type 1 diabetes
Mazaika, P. K., Marzelli, M., Tong, G., Foland‐Ross, L. C., Buckingham, B. A., Aye, T., & Reiss, A. L. (2020) · Pediatric Diabetes · doi:10.1111/pedi.12992 · Cited by 12 · see citing works
RETRACTED: Maternal diabetes-induced alterations in the expression of brain-derived neurotrophic factor in the developing rat hippocampus
Sardar, R., Hami, J., Soleimani, M., Joghataei, M. T., Shirazi, R., Golab, F., Namjoo, Z., & Zandieh, Z. (2021) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2021.101946 · Cited by 12 · see citing works
Retracted
The effect of poor glycemic control on cognitive function in children and adolescents with type 1 diabetes mellitus
Al-Shehaili, S. M., Al-Johani, S. S., Al-Sarhan, N. T., Alanazi, A. O., Almijmaj, F. F., Al-Qhatani, W. N., Al-Nasser, L. M., Al-Yami, D. R., & Al-Razooq, A. S. (2023) · Saudi Medical Journal · doi:10.15537/smj.2023.44.20230327 · Cited by 11 · see citing works
Association of attention deficit hyperactivity disorder with recurrent hypoglycemia in type 1 diabetes mellitus
Lin, S.-Y., Lin, C., Hsu, W., Lin, C., & Fu, Y. (2018) · Pediatric Diabetes · doi:10.1111/pedi.12716 · Cited by 11 · see citing works
Presence of White Matter Lesions Associated with Diabetes-Associated Cognitive Decline in Male Rat Models of Pre-Type 2 Diabetes
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Meta-analysis, A., Gaudieri, P. A., Chen, R., Greer, T. F., & Holmes, C. S. (2013)
Neuro-cognitive Performance in Children with Type 1 Diabetes—A Meta-analysis
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Authors: Tonoli, C., Heyman, E., Roelands, B., Pattyn, N., Buyse, L., Piacentini, M. F., Berthoin, S., & Meeusen, R.
Affiliations: Vrije Universiteit Brussel (BE)
Université Lille Nord de France (FR)
Corresponding author: Meeusen, Romain
ORCID: Tonoli, Cajsa
Heyman, Elsa
Roelands, Bart
Pattyn, Nathalie
Buyse, Luk
Piacentini, Maria Francesca
Berthoin, Serge
Meeusen, Romain
Venue: Journal of Diabetes
Publisher: Wiley
Published: 2014-09-10
Volume: 6
Issue: 6
Pages: 499-513
ISSN: 1753-0393 (ISSN-L)
1753-0407
DOI: 10.1111/1753-0407.12193
OpenAlex: W1553269373
Cited by: 148
References: 98
Citations by year: 2026: 7 · 2025: 7 · 2024: 12 · 2023: 12 · 2022: 13 · 2021: 9 · 2020: 14 · 2019: 15 · 2018: 21 · 2017: 15 · 2016: 15 · 2015: 5 · 2014: 2
FWCI: 1.96
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Journal of Diabetes (publishedVersion)
PubMed (publishedVersion)
ResearchOnline - JCU (James Cook University) (submittedVersion)
HAL (submittedVersion)
LillOA (Université de Lille (University Of Lille)) (submittedVersion)
Lirias (submittedVersion)
VUBIR (Vrije Universiteit Brussel) (submittedVersion)
Funders: Vlaamse regering
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Education
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
Keywords: type 1 diabetes, cognitive decline, executive function, intelligence quotient, motor speed, memory, severe hypoglycemia, chronic hyperglycemia, age of onset, diabetes duration, children versus adults, diabetes complications
MeSH terms: Adult, Age Factors, Child, Cognition, Cognition Disorders, Diabetes Mellitus, Type 1, Humans, Memory, Neuropsychological Tests, Severity of Illness Index

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Type 1 diabetes‐associated cognitive decline: A meta‐analysis and update of the current literature 1型糖尿病相关的认知能力下降：一项对最新文献的meta分析

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