Altered Brain Regional Homogeneity in First-Degree Relatives of Type
                    2 Diabetics: A functional MRI Study

Yiyong Liu; Lin Shi; Xiubao Song; Changzheng Shi; Wutao Lou; Dong Zhang; Alan D. Wang; Liangping Luo

doi:10.1055/a-0883-4955

Experimental and Clinical Endocrinology & Diabetes, Table of Contents

Exp Clin Endocrinol Diabetes 2020; 128(11): 737-744
DOI: 10.1055/a-0883-4955

Article

Altered Brain Regional Homogeneity in First-Degree Relatives of Type 2 Diabetics: A functional MRI Study

Yiyong Liu

¹Medical Imaging Center, the First Affiliated Hospital of Jinan University, Guangzhou, China

,

Lin Shi

³Department of Imaging and Interventional Radiology, Research Centre for Medical Image Computing, The Chinese University of Hong Kong, China

⁴Chow Yuk Ho Technology Centre for Innovative Medicine, The Chinese University of Hong Kong, China

,

Xiubao Song

²Department of Rehabilitation, the First Affiliated Hospital of Jinan University, Guangzhou, China

,

Changzheng Shi

¹Medical Imaging Center, the First Affiliated Hospital of Jinan University, Guangzhou, China

,

Wutao Lou

³Department of Imaging and Interventional Radiology, Research Centre for Medical Image Computing, The Chinese University of Hong Kong, China

,

Dong Zhang

¹Medical Imaging Center, the First Affiliated Hospital of Jinan University, Guangzhou, China

,

Alan D. Wang

⁵Auckland Bioengineering Institute, and Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand

⁶Shenzhen SmartView MedTech Limited, Shenzhen, China

,

Liangping Luo

¹Medical Imaging Center, the First Affiliated Hospital of Jinan University, Guangzhou, China

› Author Affiliations

Abstract

Objective This study aimed to investigate regional homogeneity in the first-degree relatives of type 2 diabetes patients.

Methods Seventy-eight subjects, including 26 type 2 diabetes patients, 26 first-degree relatives, and 26 healthy controls, were assessed. All participants underwent resting-state functional magnetic resonance imaging scanning. The estimated regional homogeneity value was used to evaluate differences in brain activities.

Results In first-degree relatives, we observed significantly decreased regional homogeneity in the left anterior cingulate cortex, left insula, and bilateral temporal lobes, and increased regional homogeneity in the left superior frontal gyrus, right anterior cingulate cortex, and bilateral posterior cingulate cortex compared to healthy controls. In type 2 diabetes patients, we detected altered regional homogeneity in the left anterior cingulate cortex, left insula, bilateral posterior cingulate cortex, and several other brain regions compared to healthy controls. Both first-degree relatives and type 2 diabetes patients showed decreased regional homogeneity in the left superior temporal gyrus, right middle temporal gyrus, left anterior cingulate cortex, left insula, and increased regional homogeneity in the left superior frontal gyrus and bilateral posterior cingulate cortex.

Conclusion These findings suggest that altered regional homogeneity in the left anterior cingulate cortex, left insula, left superior frontal gyrus, bilateral posterior cingulate cortex, and bilateral temporal lobes might be a neuroimaging biomarker of type 2 diabetes -related brain dysfunction.

Key words

first-degree relatives - type 2 diabetes - cognitive performance - resting-state functional magnetic resonance imaging - regional homogeneity

Full Text

References

References
1 Ogurtsova K, da Rocha Fernandes JD, Huang Y. et al. IDF Diabetes Atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 2017; 128: 40-50
2 Prasad RB, Groop L. Genetics of type 2 diabetes-pitfalls and possibilities. Genes. Basel; 2015: 6: 87–123
3 Kahn CR, Vicent D, Doria A. Genetics of non-insulin-dependent (type-II) diabetes mellitus. Annu Rev Med 1996; 47: 509-531
4 Anthanont P, Ramos P, Jensen MD et al. Family history of type 2 diabetes, abdominal adipocyte size and markers of the metabolic syndrome. Int J Obes (Lond) 2017
5 Alberti KGMM, Zimmet P, Shaw J. International Diabetes Federation: A consensus on Type 2 diabetes prevention. Diabetic Med 2007; 24: 451-463
6 Gaulton KJ. Mechanisms of Type 2 Diabetes Risk Loci. Curr Diab Rep 2017; 17: 72
7 Lau W, Andrew T, Maniatis N. High-resolution genetic maps identify multiple type 2 diabetes loci at regulatory hotspots in African Americans and Europeans. Am J Hum Genet 2017; 100: 803-816
8 Saczynski JS, Jonsdottir MK, Garcia ME. et al. Cognitive impairment: An increasingly important complication of type 2 diabetes: The age, gene/environment susceptibility – Reykjavik study. American Journal of Epidemiology 2008; 168: 1132-1139
9 Dybjer E, Nilsson PM, Engstrom G. et al. Pre-diabetes and diabetes are independently associated with adverse cognitive test results: A cross-sectional, population-based study. BMC endocrine disorders 2018; 18: 91
10 Biessels GJ, Despa F. Cognitive decline and dementia in diabetes mellitus: mechanisms and clinical implications. Nat Rev Endocrinol 2018; 14: 591-604
11 Tsai JC, Chen CW, Chu H. et al. Comparing the sensitivity, specificity, and predictive values of the montreal cognitive assessment and mini-mental state examination when screening people for mild cognitive impairment and dementia in chinese population. Archives of psychiatric nursing 2016; 30: 486-491
12 Petermann F, Troncoso-Pantoja C, Martinez MA. et al. [Risk of cognitive impairment among older people with diabetes or family history of the disease]. Revista medica de Chile 2018; 146: 872-881
13 Wang YF, Ji XM, Lu GM. et al. Resting-state functional MR imaging shed insights into the brain of diabetes. Metab Brain Dis 2016; 31: 993-1002
14 Zang Y, Jiang T, Lu Y. et al. Regional homogeneity approach to fMRI data analysis. Neuroimage 2004; 22: 394-400
15 Jiang L, Zuo XN. Regional homogeneity: A multimodal, multiscale neuroimaging marker of the human connectome. Neuroscientist 2016; 22: 486-505
16 Liu D, Duan S, Zhang J. et al. Aberrant brain regional homogeneity and functional connectivity in middle-aged t2dm patients: a resting-state functional mri study. Front Hum Neurosci 2016; 10: 490
17 Peng J, Qu H, Peng J. et al. Abnormal spontaneous brain activity in type 2 diabetes with and without microangiopathy revealed by regional homogeneity. Eur J Radiol 2016; 85: 607-615
18 Janghorbani M, Amini M. Progression to impaired glucose metabolism in first-degree relatives of patients with type 2 diabetes in Isfahan, Iran. Diabetes Metab Res Rev 2009; 25: 748-755
19 Assoc AD. Standards of Medical Care in Diabetes-2010. Diabetes Care 2010; 33: S11-S61
20 Chao-Gan Y, Yu-Feng Z. DPARSF: A MATLAB Toolbox for "Pipeline" Data Analysis of Resting-State fMRI. Front Syst Neurosci 2010; 4: 13
21 Kendall MG. Rank correlation methods. Oxford, England: Griffin; 1948
22 Musen G, Jacobson AM, Bolo NR. et al. Resting-state brain functional connectivity is altered in type 2 diabetes. Diabetes 2012; 61: 2375-2379
23 Xia W, Chen YC, Ma J. Resting-state brain anomalies in type 2 diabetes: A meta-analysis. Front Aging Neurosci 2017; 9: 14
24 Lopez-Larson MP, Anderson JS, Ferguson MA. et al. Local brain connectivity and associations with gender and age. Dev Cogn Neurosci 2011; 1: 187-197
25 Bernier M, Croteau E, Castellano CA. et al. Spatial distribution of resting-state BOLD regional homogeneity as a predictor of brain glucose uptake: A study in healthy aging. Neuroimage 2017; 150: 14-22
26 Landau SM, Mintun MA, Joshi AD. et al. Amyloid deposition, hypometabolism, and longitudinal cognitive decline. Ann Neurol 2012; 72: 578-586
27 Duarte JMN. Metabolic alterations associated to brain dysfunction in diabetes. Aging Dis 2015; 6: 304-321
28 Whitmer RA. Type 2 diabetes and risk of cognitive impairment and dementia. Curr Neurol Neurosci Rep 2007; 7: 373-380
29 Strachan MW, Reynolds RM, Marioni RE. et al. Cognitive function, dementia and type 2 diabetes mellitus in the elderly. Nat Rev Endocrinol 2011; 7: 108-114
30 Koekkoek PS, Biessels GJ, Kooistra M. et al. Undiagnosed cognitive impairment, health status and depressive symptoms in patients with type 2 diabetes. J Diabetes Complications 2015; 29: 1217-1222
31 Menon V, Uddin LQ. Saliency, switching, attention and control: A network model of insula function. Brain Struct Funct 2010; 214: 655-667
32 Wijngaarden MA, Veer IM, Rombouts SARB. et al. Obesity is marked by distinct functional connectivity in brain networks involved in food reward and salience. Behav Brain Res 2015; 287: 127-134
33 Lopez-Larson MP, King JB, Terry J. et al. Reduced insular volume in attention deficit hyperactivity disorder. Psychiatry Res 2012; 204: 32-39
34 Steward T, Pico-Perez M, Mata F. et al. Emotion regulation and excess weight: Impaired affective processing characterized by dysfunctional insula activation and connectivity. PLoS One 2016; 11: e0152150
35 Kann S, Zhang S, Manza P. et al. Hemispheric lateralization of resting-state functional connectivity of the anterior insula: association with age, gender, and a novelty-seeking trait. Brain Connect 2016; 6: 724-734
36 Leech R, Sharp DJ. The role of the posterior cingulate cortex in cognition and disease. Brain 2014; 137: 12-32
37 Cui Y, Jiao Y, Chen YC. et al. Altered spontaneous brain activity in type 2 Diabetes: A Resting-state functional MRI Study. . Diabetes 2014; 63: 749-760
38 Gold SM, Dziobek I, Sweat V. et al. Hippocampal damage and memory impairments as possible early brain complications of type 2 diabetes. Diabetologia 2007; 50: 711-719
39 Xia W, Wang S, Sun Z. et al. Altered baseline brain activity in type 2 diabetes: A resting-state fMRI study. Psychoneuroendocrinology 2013; 38: 2493-2501
40 van Schie HT, Wijers AA, Mars RB. et al. Processing of visual semantic information to concrete words: Temporal dynamics and neural mechanisms indicated by event-related brain potentials. Cogn Neuropsychol 2005; 22: 364-386
41 Goldberg II, Harel M, Malach R. When the brain loses its self: Prefrontal inactivation during sensorimotor processing. Neuron 2006; 50: 329-339
42 Macpherson H, Formica M, Harris E. et al. Brain functional alterations in Type 2 Diabetes - A systematic review of fMRI studies. Front Neuroendocrinol 2017; 47: 34-46