Long-term changes in insula-mesolimbic structural and functional connectivity in obese patients after laparoscopic sleeve gastrectomy

Hao Li; Yang Hu; Guanya Li; Wenchao Zhang; Jia Wang; Zongxin Tan; Zhenzhen Jia; Lei Zhang; Shuai Lv; Juan Yu; Yu Han; Guangbin Cui; Peter Manza; Nora D Volkow; Yongzhan Nie; Gang Ji; Gene-Jack Wang; Yi Zhang

doi:10.1007/s10286-022-00877-y

Long-term changes in insula-mesolimbic structural and functional connectivity in obese patients after laparoscopic sleeve gastrectomy

Clin Auton Res. 2022 Aug;32(4):237-247. doi: 10.1007/s10286-022-00877-y. Epub 2022 Jul 21.

Authors

Hao Li^#^{1

2

3}, Yang Hu^#^{1

2

3}, Guanya Li^{1

2

3}, Wenchao Zhang^{1

2

3}, Jia Wang^{1

2

3}, Zongxin Tan^{1

2

3}, Zhenzhen Jia^{1

2

3}, Lei Zhang^{1

2

3}, Shuai Lv^{1

2

3}, Juan Yu⁴, Yu Han⁵, Guangbin Cui⁵, Peter Manza⁶, Nora D Volkow⁶, Yongzhan Nie⁴, Gang Ji^#⁷, Gene-Jack Wang⁸, Yi Zhang^{9

10

11}

Affiliations

¹ Center for Brain Imaging, School of Life Science and Technology, Xidian University, Xi'an, 710071, Shaanxi, China.
² Engineering Research Center of Molecular and Neuro Imaging, Ministry of Education, Xi'an, 710126, Shaanxi, China.
³ International Joint Research Center for Advanced Medical Imaging and Intelligent Diagnosis and Treatment and Xi'an Key Laboratory of Intelligent Sensing and Regulation of Trans-Scale Life Information, School of Life Science and Technology, Xidian University, Xi'an, 710126, Shaanxi, China.
⁴ State Key Laboratory of Cancer Biology, National Clinical Research Center for Digestive Diseases and Xijing Hospital of Digestive Diseases, Air Force Medical University, No. 127 Changle West Road, Xi'an, 710032, Shaanxi, China.
⁵ Department of Radiology, Tangdu Hospital, Air Force Medical University, Xi'an, 710038, Shaanxi, China.
⁶ Laboratory of Neuroimaging, National Institute On Alcohol Abuse and Alcoholism, 10 Center Drive, MSC1013, Building 10, Room B2L304, Bethesda, MD, 20892-1013, USA.
⁷ State Key Laboratory of Cancer Biology, National Clinical Research Center for Digestive Diseases and Xijing Hospital of Digestive Diseases, Air Force Medical University, No. 127 Changle West Road, Xi'an, 710032, Shaanxi, China. jigang@fmmu.edu.cn.
⁸ Laboratory of Neuroimaging, National Institute On Alcohol Abuse and Alcoholism, 10 Center Drive, MSC1013, Building 10, Room B2L304, Bethesda, MD, 20892-1013, USA. gene-jack.wang@nih.gov.
⁹ Center for Brain Imaging, School of Life Science and Technology, Xidian University, Xi'an, 710071, Shaanxi, China. yizhang@xidian.edu.cn.
¹⁰ Engineering Research Center of Molecular and Neuro Imaging, Ministry of Education, Xi'an, 710126, Shaanxi, China. yizhang@xidian.edu.cn.
¹¹ International Joint Research Center for Advanced Medical Imaging and Intelligent Diagnosis and Treatment and Xi'an Key Laboratory of Intelligent Sensing and Regulation of Trans-Scale Life Information, School of Life Science and Technology, Xidian University, Xi'an, 710126, Shaanxi, China. yizhang@xidian.edu.cn.

^# Contributed equally.

PMID: 35864386
DOI: 10.1007/s10286-022-00877-y

Abstract

Objective: Brain imaging studies have shown insula-related functional and structural abnormalities in patients with obesity. Laparoscopic sleeve gastrectomy is currently an effective procedure for treating obesity, which promotes acute recovery of brain functional and structural abnormalities in obese patients. The aim of this study was to investigate the long-term impact of laparoscopic sleeve gastrectomy on insula-related structural and functional connectivity.

Methods: Diffusion tensor imaging and resting-state functional magnetic resonance imaging were employed to investigate laparoscopic sleeve gastrectomy-induced changes in insula-related structural connectivity and corresponding resting-state functional connectivity in 25 obese patients prior to (PreLSG) and 12 months post-surgery (PostLSG₁₂).

Results: Results showed significant increases in fractional anisotropy and axial diffusivity between the right insula and anterior cingulate cortex, and higher fractional anisotropy of left insula-putamen, left insula-caudate and anterior cingulate cortex-right posterior cingulate cortex/precuneus at PostLSG12 compared with PreLSG. There were significant negative correlations between axial diffusivity of right insula-anterior cingulate cortex and body mass index, and fractional anisotropy of right insula-anterior cingulate cortex with scores on external eating at PostLSG12. Anxiety and depressive status ratings were negatively correlated with fractional anisotropy of left insula-putamen at PostLSG12. In addition, there was a significant decrease in resting-state functional connectivity between left insula and left caudate.

Conclusions: These findings demonstrate long-term changes in insula-related structural and functional connectivity abnormalities promoted by laparoscopic sleeve gastrectomy, which highlight its strong association with long-term weight loss and improvement in eating behaviors.

Keywords: Diffusion tensor imaging; Insula; Laparoscopic sleeve gastrectomy; Structural and functional connectivity.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Intramural

MeSH terms

Diffusion Tensor Imaging*
Gastrectomy
Humans
Laparoscopy*
Magnetic Resonance Imaging / methods
Obesity / diagnostic imaging
Obesity / surgery