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Deteriorated functional and structural brain networks and normally appearing functional–structural coupling in diabetic kidney disease: a graph theory-based magnetic resonance imaging study

  • Yun Fei Wang
  • Ping Gu
  • Jiong Zhang
  • Rongfeng Qi
  • Michael de Veer
  • Gang Zheng
  • Qiang Xu
  • Ya Liu
  • Guang Ming Lu
  • Long Jiang ZhangEmail author
Neuro

Abstract

Purpose

This study was conducted in order to investigate the topological organization of functional and structural brain networks in diabetic kidney disease (DKD) and its potential clinical relevance.

Methods

Two hundred two subjects (62 DKD patients, 60 diabetes mellitus [DM] patients, and 80 healthy controls) underwent laboratory examination, neuropsychological test, and magnetic resonance imaging (MRI). Large-scale functional and structural brain networks were constructed and graph theoretical network analyses were performed. The effect of renal function on brain functional and structural networks in DKD patients was further evaluated. Correlations were performed between network properties and neuropsychological scores and clinical variables.

Results

Progressing deteriorated global and local network topology organizations (especially for functional network) were observed for DKD patients compared with control subjects (all p < 0.05, Bonferroni-corrected), with intermediate values for the patients with DM. DKD patients showed normally appearing functional–structural coupling compared with controls, while DM patients manifested functional–structural decoupling (p < 0.05, Bonferroni-corrected). Impaired kidney function markedly affected functional and structural network organization in DKD patients (all p < 0.05). Urea nitrogen correlated with global and local efficiency in the structural networks (r = − 0.551, p < 0.001; r = − 0.476, p < 0.001, respectively). Global and local efficiency in the structural networks and normalized characteristic path length in the functional networks were associated with information processing speed and/or psychomotor speed.

Conclusion

DKD patients showed enhanced functional and structural brain network disruption and normally appearing functional–structural coupling compared with DM patients, which correlated with kidney function, renal toxins, and cognitive performance.

Key Points

• DKD patients showed markedly disrupted functional and structural brain network efficiency measures compared with DM patients and healthy controls.

• Reduced kidney function clearly deteriorated functional and structural brain networks in DKD patients.

• DKD patients displayed normally appearing functional–structural coupling compared with DM patients.

Keywords

Diabetic nephropathies Diabetes mellitus Diffusion tensor imaging Magnetic resonance imaging 

Abbreviations

γ

Normalized clustering coefficient

λ

Normalized characteristic path length

σ

Small-worldness

AAL

Automated anatomical labeling

ADA

American Diabetes Association

ANCOVA

Analysis of covariance

BUN

Blood urea nitrogen

Cp

Clustering coefficient

Cyst C

Cystatin C

DKD

Diabetic kidney disease

DM

Diabetes mellitus

DPARSF

Data Processing Assistant for Resting-State fMRI

DS

Deep subcortical

DTI

Diffusion tensor imaging

Eg

Global efficiency

eGFR

Estimated glomerular filtration rate

Eloc

Local efficiency

FBG

Fasting blood glucose

HbA1c

Hemoglobin A1c

HDL-C

High-density lipoprotein cholesterol

LDL-C

Low-density lipoprotein cholesterol

Lp

Characteristic path length

LTT

Line Tracing Test

MMSE

Mini-Mental State Examination

MoCA

Montreal Cognitive Assessment

MRI

Magnetic resonance imaging

NCT-A

Number Connection Test type-A

PV

Periventricular

rs-fMRI

Resting-state functional magnetic resonance imaging

SAS

Self-Rating Anxiety Scale

Scr

Serum creatinine

SDS

Self-Rating Depression Scale

SDT

Serial Dotting Test

TC

Total cholesterol

TIV

Total intracranial volume

Tri

Triglycerides

UA

Uric acid

WML

White matter lesions

Notes

Funding

This study was funded by grants from the National Natural Science Foundation of China (81322020, 81230032, 81471644).

Compliance with ethical standards

Guarantor

The scientific guarantor of this publication is Long Jiang Zhang.

Conflict of interest

The authors declare that they have no conflicts of interest.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Study subjects or cohorts overlap

Some study subjects or cohorts have not been previously reported.

Methodology

• prospective

• observational

• performed at one institution

Supplementary material

330_2019_6164_MOESM1_ESM.docx (64 kb)
ESM 1 (DOCX 63 kb)

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Copyright information

© European Society of Radiology 2019

Authors and Affiliations

  1. 1.Department of Medical Imaging, Jinling HospitalMedical School of Nanjing UniversityNanjingChina
  2. 2.Department of Endocrinology, Jinling HospitalMedical School of Nanjing UniversityNanjingChina
  3. 3.National Clinical Research Center of Kidney Disease, Jinling HospitalMedical School of Nanjing UniversityNanjingChina
  4. 4.Monash Biomedical ImagingMonash UniversityClaytonAustralia

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