与2型糖尿病胰岛素抵抗相关的皮质下脑体积和皮质厚度改变
Altered Subcortical Brain Volume and Cortical Thickness Related to Insulin Resistance in Type 2 Diabetes Mellitus
DOI: 10.12677/acm.2024.14112885, PDF,   
作者: 吕志强:黑龙江中医药大学第一临床医学院,黑龙江 哈尔滨;杜丽坤*:黑龙江中医药大学附属第一医院内分泌二科,黑龙江 哈尔滨
关键词: 脑容量皮质厚度胰岛素抵抗结构磁共振成像2型糖尿病Brain Volume Cortical Thickness Insulin Resistance Structural Magnetic Resonance Imaging Type 2 Diabetes Mellitus
摘要: 目的:本研究的目的是通过应用形态测量技术检查被诊断患有2型糖尿病(T2DM)的个体皮质下脑体积和皮质厚度的变化,此外,还调查这些修饰与胰岛素抵抗(IR)之间的潜在关联。材料和方法:本横断面研究共包括121名参与者(n = 48名健康对照[HCs]和n = 73名T2DM患者),他们被招募并接受了一系列认知测试和结构磁共振成像(MRI)。FreeSurfer用于处理MRI数据。协方差分析比较了T2DM和HCs之间皮质厚度和皮质下脑体积的差异,调整了性别、年龄、教育和体重指数(BMI)的潜在混杂效应。探索性偏相关调查了T2DM参与者IR与大脑结构之间的联系。结果:与HCs相比,T2DM患者表现出右尾额中回、右鳃盖骨、左中央前回和双侧额上回的皮质厚度减少。此外,这项针对T2DM的研究发现,IR的严重程度与左壳核和左海马体的体积以及左眶骨部、左钙质周围、右内嗅区和右喙前扣带回的厚度呈负相关。结论:观察到T2DM大脑结构变化的证据,皮质厚度的变化集中在额叶。IR和额叶皮质变薄之间的相关性可能作为T2DM的潜在神经影像学标志物,并导致各种与糖尿病相关的脑部并发症。
Abstract: Purpose: The objective of this study is to examine the alterations in subcortical brain volume and cortical thickness among individuals diagnosed with Type 2 diabetes mellitus (T2DM) through the application of morphometry techniques and, additionally, to investigate the potential association between these modifications and insulin resistance (IR). Materials and Methods: The present cross-sectional study comprised a total of 121 participants (n = 48 with healthy controls [HCs] and n = 73 with T2DM) who were recruited and underwent a battery of cognitive testing and structural magnetic resonance imaging (MRI). FreeSurfer was used to process the MRI data. Analysis of covariance compared discrepancies in cortical thickness and subcortical brain volume between T2DM and HCs, adjusting for the potential confounding effects of gender, age, education, and body mass index (BMI). Exploratory partial correlations investigated links between IR and brain structure in T2DM participants. Results: Compared with HCs, individuals with T2DM demonstrated a cortical thickness decrease in the right caudal middle frontal gyrus, right pars opercularis, left precentral gyrus, and bilateral superior frontal gyrus. Furthermore, this study for T2DM found that the severity of IR was inversely related to the volume of the left putamen and left hippocampus, as well as the thickness of the left pars orbitalis, left pericalcarine, right entorhinal area, and right rostral anterior cingulate gyrus. Conclusion: The evidence for structural brain changes in T2DM was observed, and alterations in cortical thickness were concentrated in the frontal lobes. Correlations between IR and frontal cortical thinning may serve as a potential neuroimaging marker of T2DM and lead to various diabetes-related brain complications.
文章引用:吕志强, 杜丽坤. 与2型糖尿病胰岛素抵抗相关的皮质下脑体积和皮质厚度改变[J]. 临床医学进展, 2024, 14(11): 342-349. https://doi.org/10.12677/acm.2024.14112885

参考文献

[1] Agrawal, R., Reno, C.M., Sharma, S., Christensen, C., Huang, Y. and Fisher, S.J. (2021) Insulin Action in the Brain Regulates both Central and Peripheral Functions. American Journal of Physiology-Endocrinology and Metabolism, 321, E156-E163. [Google Scholar] [CrossRef] [PubMed]
[2] American Diabetes Association (2020) 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes—2021. Diabetes Care, 44, S15-S33. [Google Scholar] [CrossRef] [PubMed]
[3] Barnes, J., Ridgway, G.R., Bartlett, J., Henley, S.M.D., Lehmann, M., Hobbs, N., et al. (2010) Head Size, Age and Gender Adjustment in MRI Studies: A Necessary Nuisance? NeuroImage, 53, 1244-1255. [Google Scholar] [CrossRef] [PubMed]
[4] Bernardes, G., IJzerman, R.G., ten Kulve, J.S., Barkhof, F., Diamant, M., Veltman, D.J., et al. (2018) Cortical and Subcortical Gray Matter Structural Alterations in Normoglycemic Obese and Type 2 Diabetes Patients: Relationship with Adiposity, Glucose, and Insulin. Metabolic Brain Disease, 33, 1211-1222. [Google Scholar] [CrossRef] [PubMed]
[5] Brundel, M., van den Heuvel, M., de Bresser, J., Kappelle, L.J. and Biessels, G.J. (2010) Cerebral Cortical Thickness in Patients with Type 2 Diabetes. Journal of the Neurological Sciences, 299, 126-130. [Google Scholar] [CrossRef] [PubMed]
[6] Callisaya, M.L., Beare, R., Moran, C., Phan, T., Wang, W. and Srikanth, V.K. (2018) Type 2 Diabetes Mellitus, Brain Atrophy and Cognitive Decline in Older People: A Longitudinal Study. Diabetologia, 62, 448-458. [Google Scholar] [CrossRef] [PubMed]
[7] Cheng, C.P., Cheng, S., Tam, C.W., Chan, W., Chu, W.C. and Lam, L.C. (2018) Relationship between Cortical Thickness and Neuropsychological Performance in Normal Older Adults and Those with Mild Cognitive Impairment. Aging and disease, 9, 1020-1030. [Google Scholar] [CrossRef] [PubMed]
[8] Cui, D., Liu, X., Liu, M., Cao, W., Xue, Y., Guo, Y., et al. (2019) Subcortical Gray Matter Structural Alterations in Prediabetes and Type 2 Diabetes. NeuroReport, 30, 441-445. [Google Scholar] [CrossRef] [PubMed]
[9] Cui, Y., Tang, T., Lu, C. and Ju, S. (2022) Insulin Resistance and Cognitive Impairment: Evidence from Neuroimaging. Journal of Magnetic Resonance Imaging, 56, 1621-1649. [Google Scholar] [CrossRef] [PubMed]
[10] Desikan, R.S., Ségonne, F., Fischl, B., Quinn, B.T., Dickerson, B.C., Blacker, D., et al. (2006) An Automated Labeling System for Subdividing the Human Cerebral Cortex on MRI Scans into Gyral Based Regions of Interest. NeuroImage, 31, 968-980. [Google Scholar] [CrossRef] [PubMed]
[11] Frangou, S., Modabbernia, A., Williams, S.C.R., Papachristou, E., Doucet, G.E., Agartz, I., et al. (2021) Cortical Thickness across the Lifespan: Data from 17,075 Healthy Individuals Aged 3-90 Years. Human Brain Mapping, 43, 431-451. [Google Scholar] [CrossRef] [PubMed]
[12] Fuster, J.M. (2001) The Prefrontal Cortex—An Update. Neuron, 30, 319-333. [Google Scholar] [CrossRef] [PubMed]
[13] Gerlei, K.Z., Brown, C.M., Sürmeli, G. and Nolan, M.F. (2021) Deep Entorhinal Cortex: From Circuit Organization to Spatial Cognition and Memory. Trends in Neurosciences, 44, 876-887. [Google Scholar] [CrossRef] [PubMed]
[14] Hare, T.A., Camerer, C.F. and Rangel, A. (2009) Self-Control in Decision-Making Involves Modulation of the VMPFC Valuation System. Science, 324, 646-648. [Google Scholar] [CrossRef] [PubMed]
[15] Henri-Bhargava, A., Stuss, D.T. and Freedman, M. (2018) Clinical Assessment of Prefrontal Lobe Functions. CONTINUUM: Lifelong Learning in Neurology, 24, 704-726. [Google Scholar] [CrossRef] [PubMed]
[16] Hill, J.M., Lesniak, M.A., Pert, C.B. and Roth, J. (1986) Autoradiographic Localization of Insulin Receptors in Rat Brain: Prominence in Olfactory and Limbic Areas. Neuroscience, 17, 1127-1138. [Google Scholar] [CrossRef] [PubMed]
[17] International Diabetes Federation (2021) IDF Diabetes Atlas. International Diabetes Federation.
[18] Jaeger, J. (2018) Digit Symbol Substitution Test. Journal of Clinical Psychopharmacology, 38, 513-519. [Google Scholar] [CrossRef] [PubMed]
[19] Keskinoglu, P., Ucku, R., Yener, G., Yaka, E., Kurt, P. and Tunca, Z. (2009) Reliability and Validity of Revised Turkish Version of Mini Mental State Examination (RMMSE‐T) in Community‐Dwelling Educated and Uneducated Elderly. International Journal of Geriatric Psychiatry, 24, 1242-1250. [Google Scholar] [CrossRef] [PubMed]
[20] Kullmann, S., Heni, M., Hallschmid, M., Fritsche, A., Preissl, H. and Häring, H. (2016) Brain Insulin Resistance at the Crossroads of Metabolic and Cognitive Disorders in Humans. Physiological Reviews, 96, 1169-1209. [Google Scholar] [CrossRef] [PubMed]
[21] Li, C., Zuo, Z., Liu, D., Jiang, R., Li, Y., Li, H., et al. (2020) Type 2 Diabetes Mellitus May Exacerbate Gray Matter Atrophy in Patients with Early-Onset Mild Cognitive Impairment. Frontiers in Neuroscience, 14, Article No. 85. [Google Scholar] [CrossRef] [PubMed]
[22] Li, X., Jia, S., Zhou, Z., Jin, Y., Zhang, X., Hou, C., et al. (2018) The Role of the Montreal Cognitive Assessment (MoCA) and Its Memory Tasks for Detecting Mild Cognitive Impairment. Neurological Sciences, 39, 1029-1034. [Google Scholar] [CrossRef] [PubMed]
[23] Lisman, J., Buzsáki, G., Eichenbaum, H., Nadel, L., Ranganath, C. and Redish, A.D. (2017) Viewpoints: How the Hippocampus Contributes to Memory, Navigation and Cognition. Nature Neuroscience, 20, 1434-1447. [Google Scholar] [CrossRef] [PubMed]
[24] Kharabian Masouleh, S., Eickhoff, S.B., Hoffstaedter, F. and Genon, S. (2019) Empirical Examination of the Replicability of Associations between Brain Structure and Psychological Variables. eLife, 8, e43464. [Google Scholar] [CrossRef] [PubMed]
[25] Mateen, B.A., Bussas, M., Doogan, C., Waller, D., Saverino, A., Király, F.J., et al. (2018) The Trail Making Test: A Study of Its Ability to Predict Falls in the Acute Neurological In-Patient Population. Clinical Rehabilitation, 32, 1396-1405. [Google Scholar] [CrossRef] [PubMed]
[26] Matsuda, M. and DeFronzo, R.A. (1999) Insulin Sensitivity Indices Obtained from Oral Glucose Tolerance Testing: Comparison with the Euglycemic Insulin Clamp. Diabetes Care, 22, 1462-1470. [Google Scholar] [CrossRef] [PubMed]
[27] van Wouwe, N.C., Neimat, J.S., van den Wildenberg, W.P.M., Hughes, S.B., Lopez, A.M., Phibbs, F.T., et al. (2020) Subthalamic Nucleus Subregion Stimulation Modulates Inhibitory Control. Cerebral Cortex Communications, 1, tgaa083. [Google Scholar] [CrossRef] [PubMed]
[28] Moran, C., Phan, T.G., Chen, J., Blizzard, L., Beare, R., Venn, A., et al. (2013) Brain Atrophy in Type 2 Diabetes: Regional Distribution and Influence on Cognition. Diabetes Care, 36, 4036-4042. [Google Scholar] [CrossRef] [PubMed]
[29] Moulton, C.D., Costafreda, S.G., Horton, P., Ismail, K. and Fu, C.H.Y. (2015) Meta-Analyses of Structural Regional Cerebral Effects in Type 1 and Type 2 Diabetes. Brain Imaging and Behavior, 9, 651-662. [Google Scholar] [CrossRef] [PubMed]
[30] Park, S.Y., Gautier, J. and Chon, S. (2021) Assessment of Insulin Secretion and Insulin Resistance in Human. Diabetes & Metabolism Journal, 45, 641-654. [Google Scholar] [CrossRef] [PubMed]
[31] Peng, B., Chen, Z., Ma, L. and Dai, Y. (2015) Cerebral Alterations of Type 2 Diabetes Mellitus on MRI: A Pilot Study. Neuroscience Letters, 606, 100-105. [Google Scholar] [CrossRef] [PubMed]
[32] Pizzagalli, D.A. (2014) Depression, Stress, and Anhedonia: Toward a Synthesis and Integrated Model. Annual Review of Clinical Psychology, 10, 393-423. [Google Scholar] [CrossRef] [PubMed]
[33] Shim, Y.S., Yang, D.W., Kim, H., Park, Y.H. and Kim, S. (2017) RETRACTED ARTICLE: Characteristic Differences in the Mini-Mental State Examination Used in Asian Countries. BMC Neurology, 17, Article No. 141. [Google Scholar] [CrossRef] [PubMed]
[34] Sripetchwandee, J., Chattipakorn, N. and Chattipakorn, S.C. (2018) Links between Obesity-Induced Brain Insulin Resistance, Brain Mitochondrial Dysfunction, and Dementia. Frontiers in Endocrinology, 9, Article No. 496. [Google Scholar] [CrossRef] [PubMed]
[35] Gilbert, J.R., Ballard, E.D., Galiano, C.S., Nugent, A.C. and Zarate, C.A. (2020) Magnetoencephalographic Correlates of Suicidal Ideation in Major Depression. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 5, 354-363. [Google Scholar] [CrossRef] [PubMed]
[36] Stuss, D.T. (2008) Rehabilitation of Frontal Lobe Dysfunction: A Working Framework. In: Oddy, M. and Worthington, A., Eds., Rehabilitation of Executive Disorders, Oxford University Press, 3-18. [Google Scholar] [CrossRef
[37] Tolle, K.A., Rahman-Filipiak, A.M., Hale, A.C., Kitchen Andren, K.A. and Spencer, R.J. (2019) Grooved Pegboard Test as a Measure of Executive Functioning. Applied Neuropsychology: Adult, 27, 414-420. [Google Scholar] [CrossRef] [PubMed]
[38] Yang, J.J. (2022) Brain Insulin Resistance and the Therapeutic Value of Insulin and Insulin-Sensitizing Drugs in Alzheimer’s Disease Neuropathology. Acta Neurologica Belgica, 122, 1135-1142. [Google Scholar] [CrossRef] [PubMed]
[39] Zhao, Q., Guo, Q., Liang, X., Chen, M., Zhou, Y., Ding, D., et al. (2015) Auditory Verbal Learning Test Is Superior to Rey-Osterrieth Complex Figure Memory for Predicting Mild Cognitive Impairment to Alzheimer’s Disease. Current Alzheimer Research, 12, 520-526. [Google Scholar] [CrossRef] [PubMed]
[40] Zheng, Y., Ley, S.H. and Hu, F.B. (2017) Global Aetiology and Epidemiology of Type 2 Diabetes Mellitus and Its Complications. Nature Reviews Endocrinology, 14, 88-98. [Google Scholar] [CrossRef] [PubMed]
[41] Zilliox, L.A., Chadrasekaran, K., Kwan, J.Y. and Russell, J.W. (2016) Diabetes and Cognitive Impairment. Current Diabetes Reports, 16, Article No. 87. [Google Scholar] [CrossRef] [PubMed]
[42] Monereo-Sánchez, J., Jansen, J.F.A., Köhler, S., van Boxtel, M.P.J., Backes, W.H., Stehouwer, C.D.A., et al. (2023) The Association of Prediabetes and Type 2 Diabetes with Hippocampal Subfields Volume: The Maastricht Study. NeuroImage: Clinical, 39, Article ID: 103455. [Google Scholar] [CrossRef] [PubMed]