UDC

616-036

DOI

10.37482/2687-1491-Z199

Authors

Yuri V. Bykov*/** ORCID: https://orcid.org/0000-0003-4705-3823
*Stavropol State Medical University (Stavropol, Russia)
**K.G. Filippsky City Children’s Clinical Hospital (Stavropol, Russia)

Corresponding author: Yuri Bykov, address: ul. Mira 310, Stavropol, 355003, Russia; e-mail: yubykov@gmail.com

Abstract

Type 1 diabetes mellitus (DM) is a common childhood endocrinopathy that can present with cognitive dysfunction (CD). PubMed, Cochrane Library, eLIBRARY.RU and Medscape databases were searched for Englishand Russian-language articles published from 2010 to 2023 using the following keywords: type 1 diabetes mellitus, children, cognitive dysfunction and diagnosis. Publications on CD in adult patients with type 1 DM were excluded from this review. In children with DM, the aetiology of CD is multifactorial and has the following confirmed risk factors: acute hypoglycaemia, chronic hyperglycaemia, early DM onset and pronounced diabetic ketoacidosis. CD manifests clinically with declined memory, attention, IQ scores, psychomotor reactions and cognitive flexibility. In children with an early disease onset (before the age of 6), CD manifestations are more pronounced. The neuropsychological methods considered part of the gold standard for CD diagnosis in children are: the Stroop Colour and Word Test, Benton Visual Retention Test, Wechsler Intelligence Scale for Children, and Wisconsin Card Sorting Test. The representative instrumental methods include magnetic resonance imaging, electroencephalography, diffusion tensor imaging, etc. They allow us to assess the anatomical and functional changes in the brain of children with type 1 DM. Laboratory-based methods can detect an increase in neurospecific proteins and inflammation markers, which indicates cerebral damage in patients with the disease. Further research is necessary on type 1 DM-associated CD in paediatric practice in order to improve the diagnostic criteria for this complication and its prevention methods.

Keywords

children with type 1 diabetes mellitus, cognitive dysfunction, diagnosis of brain disorders, neurospecific proteins, neuropsychological testing, neuroimaging

References

1. Pourabbasi A., Tehrani-Doost M., Ebrahimi Qavam S., Larijani B. Evaluation of the Correlation Between Type 1 Diabetes and Cognitive Function in Children and Adolescents, and Comparison of This Correlation with Structural Changes in the Central Nervous System: A Study Protocol. BMJ Open, 2016, vol. 6, no. 4. Art. no. e007917.
https://doi.org/10.1136/bmjopen-2015-007917
2. Lancrei H.M., Yeshayahu Y., Grossman E.S., Berger I. Sweet but Sour: Impaired Attention Functioning in Children with Type 1 Diabetes Mellitus. Front. Hum. Neurosci., 2022, vol. 16. Art. no. 895835. https://doi.org/10.3389/fnhum.2022.895835
3. Bykov YuV. Cognitive Disorders Analysis in Children with Diabetes Mellitus Type I Depending on the Stage of the Disease. Bull. Contemp. Clin. Med., 2021, vol. 14, no. 2, pp. 12–15 (in Russ.). https://doi.org/10.20969/VSKM.2021.14(2).12-15
4. Bykov Yu.V., Baturin V.A. Cognitive Impairments in Type 1 Diabetes Mellitus. Sib. Sci. Med. J., 2023, vol. 43, no. 1, pp. 4–12 (in Russ.). https://doi.org/10.18699/SSMJ20230101
5. Litmanovitch E., Geva R., Rachmiel M. Short and Long Term Neuro-Behavioral Alterations in Type 1 Diabetes Mellitus Pediatric Population. World J. Diabetes, 2015, vol. 6, no. 2, pp. 259–270. https://doi.org/10.4239/wjd.v6.i2.259
6. Katsarou A., Gudbjörnsdottir S., Rawshani A., Dabelea D., Bonifacio E., Anderson B.J., Jacobsen L.M., Schatz D.A., Lernmark Å. Type 1 Diabetes Mellitus. Nat. Rev. Dis. Primers, 2017, vol. 3. Art. no. 17016. https://doi.org/10.1038/nrdp.2017.16
7. Foland-Ross L.C., Buckingam B., Mauras N., Arbelaez A.M., Tamborlane W.V., Tsalikian E., Cato A., Tong G., Englert K., Mazaika P.K., Reiss A.L. Executive Task-Based Brain Function in Children with Type 1 Diabetes: An
Observational Study. PLoS Med., 2019, vol. 16, no. 12. Art. no. e1002979. https://doi.org/10.1371/journal.pmed.1002979
8. Chen H.-J., Lee Y.-J., Huang C.-C., Lin Y.-F., Li S.-T. Serum Brain-Derived Neurotrophic Factor and Neurocognitive Function in Children with Type 1 Diabetes. J. Formos. Med. Assoc., 2021, vol. 120, no. 1, pt. 1, pp. 157–164. https://doi.org/10.1016/j.jfma.2020.04.011
9. DiMeglio L.A., Evans-Molina C., Oram R.A. Type 1 Diabetes. Lancet, 2018, vol. 391, no. 10138, pp. 2449–2462. https://doi.org/10.1016/s0140-6736(18)31320-5
10. Toprak H., Yetis H., Alkan A., Filiz M., Kurtcan S., Aralasmak A., Aksu M.Ş., Cesur Y. Relationships of DTI Findings with Neurocognitive Dysfunction in Children with Type 1 Diabetes Mellitus. Br. J. Radiol., 2016, vol. 89, no. 1059. Art. no. 20150680. https://doi.org/10.1259/bjr.20150680
11. Hardigan T., Ward R., Ergul A. Cerebrovascular Complications of Diabetes: Focus on Cognitive Dysfunction. Clin. Sci. (Lond.), 2016, vol. 130, no. 20, pp. 1807–1822. https://doi.org/10.1042/cs20160397
12. Shalimova A., Graff B., Gąsecki D., Wolf J., Sabisz A., Szurowska E., Jodzio K., Narkiewicz K. Cognitive Dysfunction in Type 1 Diabetes Mellitus. J. Clin. Endocrinol. Metab., 2019, vol. 104, no. 6, pp. 2239–2249. https://doi.org/10.1210/jc.2018-01315
13. Samoylova Yu.G., Rotkank M.A., Zhukova N.G., Matveeva M.V., Tolmachev I.V., Kudlay D.A. Markery kognitivnykh narusheniy i variabel’nost’ glikemii u patsientov s sakharnym diabetom 1-go tipa [Markers for Cognitive Impairments and Variability of Glycaemia in Patients with Type 1 Diabetes Mellitus]. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova, 2018, vol. 118, no. 4, pp. 48–51. https://doi.org/10.17116/jnevro20181184148-51
14. Cato A., Hershey T. Cognition and Type 1 Diabetes in Children and Adolescents. Diabetes Spectr., 2016, vol. 29, no. 4, pp. 197–202. https://doi.org/10.2337/ds16-0036
15. Jaser S.S., Jordan L.C. Brain Health in Children with Type 1 Diabetes: Risk and Protective Factors. Curr. Diabetes Rep., 2021, vol. 21, no. 4. Art. no. 12. https://doi.org/10.1007/s11892-021-01380-w
16. Pujar M., Vastrad B., Kavatagimath S., Vastrad C., Kotturshetti S. Identification of Candidate Biomarkers and Pathways Associated with Type 1 Diabetes Mellitus Using Bioinformatics Analysis. Sci. Rep., 2022, vol. 12, no. 1. Art. no. 9157. https://doi.org/10.1038/s41598-022-13291-1
17. Seaquist E.R. The Impact of Diabetes on Cerebral Structure and Function. Psychosom. Med., 2015, vol. 77, no. 6, pp. 616–621. https://doi.org/10.1097/psy.0000000000000207
18. Matveeva M.V., Samoylova Yu.G., Zhukova N.G., Kudlay D.A., Rotkank M.A., Leyman O.P. Redkie geneticheskie markery kognitivnykh narusheniy pri sakharnom diabete [Rare Genetic Markers of Cognitive Impairment in Diabetes Mellitus]. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova, 2019, vol. 119, no. 2, pp. 76–79. https://doi.org/10.17116/jnevro201911902176
19. Barnea-Goraly N., Raman M., Mazaika P., Marzelli M., Hershey T., Weinzimer S.A., Aye T., Buckingham B., Mauras N., White N.H., Fox L.A., Tansey M., Beck R.W., Ruedy K.J., Kollman C., Cheng P., Reiss A.L. Alterations in White Matter Structure in Young Children with Type 1 Diabetes. Diabetes Care, 2014, vol. 37, no. 2, pp. 332–340. https://doi.org/10.2337/dc13-1388
20. Cameron F.J., Northam E.A., Ryan C.M. The Effect of Type 1 Diabetes on the Developing Brain. Lancet Child Adolesc. Health, 2019, vol. 3, no. 6. pp. 427–436. https://doi.org/10.1016/s2352-4642(19)30055-0
21. Semenkovich K., Bischoff A., Doty T., Nelson S., Siller A.F., Hershey T., Arbeláez A.M. Clinical Presentation and Memory Function in Youth with Type 1 Diabetes. Pediatr. Diabetes, 2016, vol. 17, no. 7, pp. 492–499. https://doi.org/10.1111/pedi.12314
22. Broadley M.M., White M.J., Andrew B. A Systematic Review and Meta-Analysis of Executive Function Performance in Type 1 Diabetes Mellitus. Psychosom. Med., 2017, vol. 79, no. 6, pp. 684–696. https://doi.org/10.1097/psy.0000000000000460
23. Ryan C.M., van Duinkerken E., Rosano C. Neurocognitive Consequences of Diabetes. Am. Psychol., 2016, vol. 71, no. 7, pp. 563–576. https://doi.org/10.1037/a0040455
24. Samoylova Yu.G., Rotkank M.A., Zhukova N.G., Matveeva M.V., Oleynik O.A. Znachimost’ razlichnykh metodov diagnostiki kognitivnoy disfunktsii u patsientov s sakharnym diabetom 1-go tipa [Significance of the Different Methods of Diagnosis of Cognitive Dysfunction in Patients with Type 1 Diabetes Mellitus]. Lechashchiy vrach, 2016, no. 6, p. 86.
25. Abo-el-Asrar M., Andrawes N.G., Rabie M.A., Aly El-Gabry D., Khalifa A.-G., El-Sherif M., Abdel Aziz K. Cognitive Functions in Children and Adolescents with Early-Onset Diabetes Mellitus in Egypt. Appl. Neuropsychol. Child, 2018, vol. 7, no. 1, pp. 21–30. https://doi.org/10.1080/21622965.2016.1224186
26. Scarpina F., Tagini S. The Stroop Color and Word Test. Front. Psychol., 2017, vol. 8. Art. no. 557. https://doi.org/10.3389/fpsyg.2017.00557
27. Segabinazi J.D., Pawlowski J., Zanini A.M., Wagner G.P., Sbicigo J.B., Trentini C.M., Hutz C.S., de Salles J.F., Bandeira D.R. Age, Education and Intellectual Quotient Influences: Structural Equation Modeling on the Study of
Benton Visual Retention Test (BVRT). Span. J. Psychol., 2020, vol. 23. Art. no. e27. https://doi.org/10.1017/sjp.2020.30
28. Na S.D., Burns T.G. Wechsler Intelligence Scale for Children-V: Test Review. Appl. Neuropsychol. Child, 2016, vol. 5, no. 2, pp. 156–160. https://doi.org/10.1080/21622965.2015.1015337
29. Miles S., Howlett C.A., Berryman C., Nedeljkovic M., Moseley G.L., Phillipou A. Considerations for Using the Wisconsin Card Sorting Test to Assess Cognitive Flexibility. Behav. Res. Methods, 2021, vol. 53, no. 5, pp. 2083–2091. https://doi.org/10.3758/s13428-021-01551-3
30. Macedo L.B.C., Foss M.P., Galera C.A. Cognitive Impairments in Type 1 Diabetes Mellitus: Integrative Review. Psicologia: Teoria e Prática, 2023, vol. 25, no. 1. http://dx.doi.org/10.5935/1980-6906/ePTPPA14344.en
31. Glushchenko V.V., Shabanov P.D. Minimal’naya disfunktsiya mozga [Minimal Brain Dysfunction]. Moscow, 2013. 318 p.
32. Matveeva M.V., Samoilova Yu.G., Zhukova N.G., Tolmachov I.V., Brazovskiy K.S., Leiman O.P.,
Fimushkina N.Yu., Rotkank M.A. Neuroimaging Methods for Assessing the Brain in Diabetes Mellitus (Literature
Review). Bull. Sib. Med., 2020, vol. 19, no. 2, pp. 189–194. https://doi.org/10.20538/1682-0363-2020-2-189-194
33. Mazaika P.K., Weinzimer S.A., Mauras N., Buckingham B., White N.H., Tsalikian E., Hershey T., Cato A., Aye T., Fox L., Wilson D.M., Tansey M.J., Tamborlane W., Peng D., Raman M., Marzelli M., Reiss A.L. Variations
in Brain Volume and Growth in Young Children with Type 1 Diabetes. Diabetes, 2016, vol. 65, no. 2, pp. 476–485. https://doi.org/10.2337/db15-1242
34. Arbelaez A.M., Semenkovich K., Hershey T. Glycemic Extremes in Youth with T1DM: The Structural and Functional Integrity of the Developing Brain. Pediatr. Diabetes, 2013, vol. 14, no. 8, pp. 541–553. https://doi.org/10.1111/pedi.12088
35. Biessels G.J., Reijmer Y.D. Brain Changes Underlying Cognitive Dysfunction in Diabetes: What Can We Learn from MRI? Diabetes, 2014, vol. 63, no. 7, pp. 2244–2252. https://doi.org/10.2337/db14-0348
36. van Duinkerken E., Schoonheim M.M., Sanz-Arigita E.J., IJzerman R.G., Moll A.C., Snoek F.J., Ryan C.M., Klein M., Diamant M., Barkhof F. Resting-State Brain Networks in Type 1 Diabetic Patients with and Without
Microangiopathy and Their Relation to Cognitive Functions and Disease Variables. Diabetes, 2012, vol. 61, no. 7, pp. 1814–1821. https://doi.org/10.2337/db11-1358
37. Hershey T., Perantie D.C., Wu J., Weaver P.M., Black K.J., White N.H. Hippocampal Volumes in Youth with Type 1 Diabetes. Diabetes, 2010, vol. 59, no. 1, pp. 236–241. https://doi.org/10.2337/db09-1117
38. Berman J.I., Lanza M.R., Blaskey L., Edgar J.C., Roberts T.P.L. High Angular Resolution Diffusion Imaging Probabilistic Tractography of the Auditory Radiation. Am. J. Neuroradiol., 2013, vol. 34, no. 8, pp. 1573–1578.
https://doi.org/10.3174/ajnr.a3471
39. Gallardo-Moreno G.B., González-Garrido A.A., Villaseñor-Cabrera T., Alvarado-Rodríguez F.J., Ruiz-Stovel V.D., Jiménez-Maldonado M.E., Contreras-Piña N., Gómez-Velázquez F.R. Sustained Attention in Schoolchildren with Type-1 Diabetes. A Quantitative EEG Study. Clin. Neurophysiol., 2020, vol. 131, no. 10, pp. 2469–2478. https://doi.org/10.1016/j.clinph.2020.07.013
40. Rachmiel M., Cohen M., Heymen E., Lezinger M., Inbar D., Gilat S., Bistritzer T., Leshem G., Kan-Dror E., Lahat E., Ekstein D. Hyperglycemia Is Associated with Simultaneous Alterations in Electrical Brain Activity in Youths with Type 1 Diabetes Mellitus. Clin. Neurophysiol., 2016, vol. 127, no. 2, рр. 1188–1195. https://doi.org/10.1016/j.clinph.2015.07.011
41. Efimova V.L., Nikolaeva E.I., Kon’shina N.V., Golosnaya G.S. Possibility of Using Proteins as Neuroinflammation Markers to Evaluate Cognitive State of Children. Mod. Iss. Biomed., 2023, vol. 7, no. 2 (in Russ.). https://doi.org/10.24412/2588-0500-2023_07_02_6
42. Elshorbagy H.H., Barseem N.F., Elsadek A.E., Al-shokary A.H., Maksoud Y.H.A., Abdulsamea S.E., Talaat I.M., Suliman H.A., Kamal N.M., Abdelghani W.E., Azab S.M., El Din D.M.N. Serum Neuron-Specific Enolase and S100 Calcium-Binding Protein B in Pediatric Diabetic Ketoacidosis. J. Clin. Res. Pediatr. Endocrinol., 2019, vol. 11, no. 4, pp. 374–387. https://doi.org/10.4274/jcrpe.galenos.2019.2018.0280
43. Novoselova M.V., Samoylova Yu.G., Zhukova N.G. Soderzhanie neyrospetsificheskikh belkov pri kognitivnykh narusheniyakh u patsientov s sakharnym diabetom 1-go tipa [The Level of Neurospecific Proteins in Patients with Type 1 Diabetes Mellitus and Cognitive Disorders]. Klinicheskaya meditsina, 2014, vol. 92, no. 8, pp. 46–49.
44. Karavanaki K., Kakleas K., Georga S., Bartzeliotou A., Mavropoulos G., Tsouvalas M., Vogiatzi A., Papassotiriou I., Karayianni C. Plasma High Sensitivity C-Reactive Protein and Its Relationship with Cytokine Levels in Children with Newly Diagnosed Type 1 Diabetes and Ketoacidosis. Clin. Biochem., 2012, vol. 45, no. 16–17, pp. 1383–1388. https://doi.org/10.1016/j.clinbiochem.2012.05.003
45. Kawamoto E.M., Cutler R.G., Rothman S.M., Mattson M.P., Camandola S. TLR4-Dependent Metabolic Changes Are Associated with Cognitive Impairment in an Animal Model of Type 1 Diabetes. Biochem. Biophys. Res. Commun., 2014, vol. 443, no. 2, pp. 731–737. https://doi.org/10.1016/j.bbrc.2013.12.039
46. Kumar N., Singh V.B., Meena B.L., Kumar D., Saini M.L., Tiwari A. Mild Cognitive Impairment in Young Type 1 Diabetes Mellitus Patients and Correlation with Diabetes Control, Lipid Profile, and High-Sensitivity C-Reactive Protein. Indian J. Endocrinol. Metab., 2018, vol. 22, no. 6, pp. 780–784. https://doi.org/10.4103/ijem.ijem_58_18