Skip to main content
Top
Published in: Obesity Surgery 8/2018

01-08-2018 | Original Contributions

Sleeve Gastrectomy Recovering Disordered Brain Function in Subjects with Obesity: a Longitudinal fMRI Study

Authors: Panlong Li, Han Shan, Shengxiang Liang, Binbin Nie, Hua Liu, Shaofeng Duan, Qi Huang, Tianhao Zhang, Guanglong Dong, Yulin Guo, Jin Du, Hongkai Gao, Lin Ma, Demin Li, Baoci Shan

Published in: Obesity Surgery | Issue 8/2018

Login to get access

Abstract

Objective

Bariatric surgery could recover regional dysfunction of cerebral cortex. However, it is unknown whether bariatric surgery could recover the global-level dysfunction in subjects with obesity. The aim of this study was to investigate the effect of bariatric surgery on global-level dysfunction in subjects with obesity by resting-state functional magnetic resonance imaging (fMRI).

Methods

Resting-state fMRI was used to investigate dysfunction of whole-brain in 34 subjects with obesity and 34 age-and gender-matched normal-weight subjects, in which 17 subjects with obesity received sleeve gastrectomy. Fractional amplitude of low-frequency fluctuation (fALFF) and functional connectivity (FC) among the whole brain were used to estimate the brain functional differences among the preoperative subjects, postoperative subjects, and the controls.

Results

The preoperative subjects compared to controls had decreased resting-state activities in reward processing and cognitive control regions such as orbitofrontal cortex, middle frontal gyrus, superior frontal gyrus, and gyrus rectus. It was important that increased FC was also found in these regions. Correlation analysis showed that body mass index (BMI) was associated with these decreased activity and increased FC. More importantly, the dysfunction in these regions was recovered by the bariatric surgery.

Conclusions

These results suggest that bariatric surgery-induced weight loss could reverse the global-level dysfunction in subjects with obesity. The dysfunction in these regions might play a key role in the development of obesity, which might serve as a biomarker in the treatment of obesity.
Appendix
Available only for authorised users
Literature
2.
go back to reference Stoeckel LE, Weller RE, Cook 3rd EW, et al. Widespread reward-system activation in obese women in response to pictures of high-calorie foods. NeuroImage. 2008;41(2):636–47.CrossRefPubMed Stoeckel LE, Weller RE, Cook 3rd EW, et al. Widespread reward-system activation in obese women in response to pictures of high-calorie foods. NeuroImage. 2008;41(2):636–47.CrossRefPubMed
3.
go back to reference Kullmann S, Heni M, Linder K, et al. Resting-state functional connectivity of the human hypothalamus. Hum Brain Mapp. 2014;35(12):6088–96.CrossRefPubMed Kullmann S, Heni M, Linder K, et al. Resting-state functional connectivity of the human hypothalamus. Hum Brain Mapp. 2014;35(12):6088–96.CrossRefPubMed
4.
go back to reference Kullmann S, Frank S, Heni M, et al. Intranasal insulin modulates intrinsic reward and prefrontal circuitry of the human brain in lean women. Neuroendocrinology. 2012;97(2):176–82.CrossRefPubMed Kullmann S, Frank S, Heni M, et al. Intranasal insulin modulates intrinsic reward and prefrontal circuitry of the human brain in lean women. Neuroendocrinology. 2012;97(2):176–82.CrossRefPubMed
5.
go back to reference Cummings DE, Overduin J, Foster-Schubert KE. Gastric bypass for obesity: mechanisms of weight loss and diabetes resolution. J Clin Endocrinol Metab. 2004;89(6):2608–15.CrossRefPubMed Cummings DE, Overduin J, Foster-Schubert KE. Gastric bypass for obesity: mechanisms of weight loss and diabetes resolution. J Clin Endocrinol Metab. 2004;89(6):2608–15.CrossRefPubMed
6.
go back to reference Ochner CN, Gibson C, Shanik M, et al. Changes in neurohormonal gut peptides following bariatric surgery. Int J Obes. 2011;35(2):153–66.CrossRef Ochner CN, Gibson C, Shanik M, et al. Changes in neurohormonal gut peptides following bariatric surgery. Int J Obes. 2011;35(2):153–66.CrossRef
7.
go back to reference Spitznagel MB, Hawkins M, Alosco M, et al. Neurocognitive effects of obesity and bariatric surgery. Eur Eat Disord Rev : J Eat Disord Assoc. 2015;23(6):488–95.CrossRef Spitznagel MB, Hawkins M, Alosco M, et al. Neurocognitive effects of obesity and bariatric surgery. Eur Eat Disord Rev : J Eat Disord Assoc. 2015;23(6):488–95.CrossRef
8.
go back to reference Marques EL, Halpern A, Correa Mancini M, et al. Changes in neuropsychological tests and brain metabolism after bariatric surgery. J Clin Endocrinol Metab. 2014;99(11):E2347–52.CrossRefPubMed Marques EL, Halpern A, Correa Mancini M, et al. Changes in neuropsychological tests and brain metabolism after bariatric surgery. J Clin Endocrinol Metab. 2014;99(11):E2347–52.CrossRefPubMed
9.
go back to reference van de Sande-Lee S, Pereira FR, Cintra DE, et al. Partial reversibility of hypothalamic dysfunction and changes in brain activity after body mass reduction in obese subjects. Diabetes. 2011;60(6):1699–704.CrossRefPubMedPubMedCentral van de Sande-Lee S, Pereira FR, Cintra DE, et al. Partial reversibility of hypothalamic dysfunction and changes in brain activity after body mass reduction in obese subjects. Diabetes. 2011;60(6):1699–704.CrossRefPubMedPubMedCentral
10.
go back to reference Frank S, Wilms B, Veit R, et al. Altered brain activity in severely obese women may recover after Roux-en Y gastric bypass surgery. Int J Obes. 2014;38(3):341–8.CrossRef Frank S, Wilms B, Veit R, et al. Altered brain activity in severely obese women may recover after Roux-en Y gastric bypass surgery. Int J Obes. 2014;38(3):341–8.CrossRef
11.
go back to reference Wiemerslage L, Zhou W, Olivo G, et al. A resting-state fMRI study of obese females between pre- and postprandial states before and after bariatric surgery. Eur J Neurosci. 2017;45(3):333–41.CrossRefPubMed Wiemerslage L, Zhou W, Olivo G, et al. A resting-state fMRI study of obese females between pre- and postprandial states before and after bariatric surgery. Eur J Neurosci. 2017;45(3):333–41.CrossRefPubMed
12.
go back to reference Gonzalez-Castillo J, Hoy CW, Handwerker DA, et al. Tracking ongoing cognition in individuals using brief, whole-brain functional connectivity patterns. PNAS. 2015;112:8762–7.CrossRefPubMed Gonzalez-Castillo J, Hoy CW, Handwerker DA, et al. Tracking ongoing cognition in individuals using brief, whole-brain functional connectivity patterns. PNAS. 2015;112:8762–7.CrossRefPubMed
13.
go back to reference Baars BJ. The conscious access hypothesis: origins and recent evidence. Trends Cogn Sci. 2002;6(1):47–52.CrossRefPubMed Baars BJ. The conscious access hypothesis: origins and recent evidence. Trends Cogn Sci. 2002;6(1):47–52.CrossRefPubMed
15.
go back to reference Moreno-Lopez L, Contreras-Rodriguez O, Soriano-Mas C, et al. Disrupted functional connectivity in adolescent obesity. NeuroImage Clin. 2016;12:262–8.CrossRefPubMedPubMedCentral Moreno-Lopez L, Contreras-Rodriguez O, Soriano-Mas C, et al. Disrupted functional connectivity in adolescent obesity. NeuroImage Clin. 2016;12:262–8.CrossRefPubMedPubMedCentral
16.
go back to reference Zou QH, Zhu CZ, Yang Y, et al. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods. 2008;172(1):137–41.CrossRefPubMedPubMedCentral Zou QH, Zhu CZ, Yang Y, et al. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods. 2008;172(1):137–41.CrossRefPubMedPubMedCentral
17.
go back to reference Lahaye P-J, Poline J-B, Flandin G, et al. Functional connectivity: studying nonlinear, delayed interactions between BOLD signals. NeuroImage. 2003;20(2):962–74.CrossRefPubMed Lahaye P-J, Poline J-B, Flandin G, et al. Functional connectivity: studying nonlinear, delayed interactions between BOLD signals. NeuroImage. 2003;20(2):962–74.CrossRefPubMed
18.
go back to reference Tzourio-Mazoyer N, Landeau B, Papathanassiou D, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical Parcellation of the MNI MRI single-subject brain. NeuroImage. 2002;15(1):273–89.CrossRefPubMed Tzourio-Mazoyer N, Landeau B, Papathanassiou D, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical Parcellation of the MNI MRI single-subject brain. NeuroImage. 2002;15(1):273–89.CrossRefPubMed
19.
go back to reference Ferrarini L, Veer IM, Baerends E, et al. Hierarchical functional modularity in the resting-state human brain. Hum Brain Mapp. 2009;30(7):2220–31.CrossRefPubMed Ferrarini L, Veer IM, Baerends E, et al. Hierarchical functional modularity in the resting-state human brain. Hum Brain Mapp. 2009;30(7):2220–31.CrossRefPubMed
20.
go back to reference Braun U, Plichta MM, Esslinger C, et al. Test-retest reliability of resting-state connectivity network characteristics using fMRI and graph theoretical measures. NeuroImage. 2012;59(2):1404–12.CrossRefPubMed Braun U, Plichta MM, Esslinger C, et al. Test-retest reliability of resting-state connectivity network characteristics using fMRI and graph theoretical measures. NeuroImage. 2012;59(2):1404–12.CrossRefPubMed
21.
go back to reference Hendrick OM, Luo X, Zhang S, et al. Saliency processing and obesity: a preliminary imaging study of the stop signal task. Obesity. 2012;20(9):1796–802.CrossRefPubMed Hendrick OM, Luo X, Zhang S, et al. Saliency processing and obesity: a preliminary imaging study of the stop signal task. Obesity. 2012;20(9):1796–802.CrossRefPubMed
22.
go back to reference Ness A, Bruce J, Bruce A, et al. Pre-surgical cortical activation to food pictures is associated with weight loss following bariatric surgery. Surg Obes Relat Dis. 2014;10(6):1188–95.CrossRefPubMed Ness A, Bruce J, Bruce A, et al. Pre-surgical cortical activation to food pictures is associated with weight loss following bariatric surgery. Surg Obes Relat Dis. 2014;10(6):1188–95.CrossRefPubMed
23.
go back to reference Eiler 2nd WJ, Dzemidzic M, Case KR, et al. Ventral frontal satiation-mediated responses to food aromas in obese and normal-weight women. Am J Clin Nutr. 2014;99(6):1309–18.CrossRefPubMedPubMedCentral Eiler 2nd WJ, Dzemidzic M, Case KR, et al. Ventral frontal satiation-mediated responses to food aromas in obese and normal-weight women. Am J Clin Nutr. 2014;99(6):1309–18.CrossRefPubMedPubMedCentral
24.
go back to reference Batterink L, Yokum S, Stice E. Body mass correlates inversely with inhibitory control in response to food among adolescent girls: an fMRI study. NeuroImage. 2010;52(4):1696–703.CrossRefPubMedPubMedCentral Batterink L, Yokum S, Stice E. Body mass correlates inversely with inhibitory control in response to food among adolescent girls: an fMRI study. NeuroImage. 2010;52(4):1696–703.CrossRefPubMedPubMedCentral
25.
go back to reference Zhang Y, Wang J, Zhang G, et al. The neurobiological drive for overeating implicated in Prader-Willi syndrome. Brain Res. 2015;1620:72–80.CrossRefPubMed Zhang Y, Wang J, Zhang G, et al. The neurobiological drive for overeating implicated in Prader-Willi syndrome. Brain Res. 2015;1620:72–80.CrossRefPubMed
26.
go back to reference Glascher J, Adolphs R, Damasio H, et al. Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proc Natl Acad Sci U S A. 2012;109(36):14681–6.CrossRefPubMedPubMedCentral Glascher J, Adolphs R, Damasio H, et al. Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proc Natl Acad Sci U S A. 2012;109(36):14681–6.CrossRefPubMedPubMedCentral
27.
go back to reference Gross J, Woelbert E, Zimmermann J, et al. Value signals in the prefrontal cortex predict individual preferences across reward categories. J Neurosci : Off J Soc Neurosci. 2014;34(22):7580–6.CrossRef Gross J, Woelbert E, Zimmermann J, et al. Value signals in the prefrontal cortex predict individual preferences across reward categories. J Neurosci : Off J Soc Neurosci. 2014;34(22):7580–6.CrossRef
28.
29.
go back to reference Weise CM, Thiyyagura P, Reiman EM, et al. Fat-free body mass but not fat mass is associated with reduced gray matter volume of cortical brain regions implicated in autonomic and homeostatic regulation. NeuroImage. 2013;64:712–21.CrossRefPubMed Weise CM, Thiyyagura P, Reiman EM, et al. Fat-free body mass but not fat mass is associated with reduced gray matter volume of cortical brain regions implicated in autonomic and homeostatic regulation. NeuroImage. 2013;64:712–21.CrossRefPubMed
30.
31.
go back to reference Ljubisavljevic M, Maxood K, Bjekic J, et al. Long-term effects of repeated prefrontal cortex transcranial direct current stimulation (tDCS) on food craving in normal and overweight young adults. Brain Stimul. 2016;9(6):826–33.CrossRefPubMed Ljubisavljevic M, Maxood K, Bjekic J, et al. Long-term effects of repeated prefrontal cortex transcranial direct current stimulation (tDCS) on food craving in normal and overweight young adults. Brain Stimul. 2016;9(6):826–33.CrossRefPubMed
32.
go back to reference Goldman RL, Borckardt JJ, Frohman HA, et al. Prefrontal cortex transcranial direct current stimulation (tDCS) temporarily reduces food cravings and increases the self-reported ability to resist food in adults with frequent food craving. Appetite. 2011;56(3):741–6.CrossRefPubMed Goldman RL, Borckardt JJ, Frohman HA, et al. Prefrontal cortex transcranial direct current stimulation (tDCS) temporarily reduces food cravings and increases the self-reported ability to resist food in adults with frequent food craving. Appetite. 2011;56(3):741–6.CrossRefPubMed
33.
go back to reference Tuulari JJ, Karlsson HK, Antikainen O, et al. Bariatric surgery induces white and Grey matter density recovery in the morbidly obese: a voxel-based morphometric study. Hum Brain Mapp. 2016;37(11):3745–56.CrossRefPubMed Tuulari JJ, Karlsson HK, Antikainen O, et al. Bariatric surgery induces white and Grey matter density recovery in the morbidly obese: a voxel-based morphometric study. Hum Brain Mapp. 2016;37(11):3745–56.CrossRefPubMed
34.
go back to reference Tuulari JJ, Karlsson HK, Hirvonen J, et al. Weight loss after bariatric surgery reverses insulin-induced increases in brain glucose metabolism of the morbidly obese. Diabetes. 2013;62(8):2747–51.CrossRefPubMedPubMedCentral Tuulari JJ, Karlsson HK, Hirvonen J, et al. Weight loss after bariatric surgery reverses insulin-induced increases in brain glucose metabolism of the morbidly obese. Diabetes. 2013;62(8):2747–51.CrossRefPubMedPubMedCentral
35.
go back to reference Faulconbridge LF, Ruparel K, Loughead J, et al. Changes in neural responsivity to highly palatable foods following roux-en-Y gastric bypass, sleeve gastrectomy, or weight stability: an fMRI study. Obesity (Silver Spring). 2016;24(5):1054–60.CrossRefPubMedCentral Faulconbridge LF, Ruparel K, Loughead J, et al. Changes in neural responsivity to highly palatable foods following roux-en-Y gastric bypass, sleeve gastrectomy, or weight stability: an fMRI study. Obesity (Silver Spring). 2016;24(5):1054–60.CrossRefPubMedCentral
36.
go back to reference Lepping RJ, Bruce AS, Francisco A, et al. Resting-state brain connectivity after surgical and behavioral weight loss. Obesity (Silver Spring). 2015;23(7):1422–8.CrossRef Lepping RJ, Bruce AS, Francisco A, et al. Resting-state brain connectivity after surgical and behavioral weight loss. Obesity (Silver Spring). 2015;23(7):1422–8.CrossRef
Metadata
Title
Sleeve Gastrectomy Recovering Disordered Brain Function in Subjects with Obesity: a Longitudinal fMRI Study
Authors
Panlong Li
Han Shan
Shengxiang Liang
Binbin Nie
Hua Liu
Shaofeng Duan
Qi Huang
Tianhao Zhang
Guanglong Dong
Yulin Guo
Jin Du
Hongkai Gao
Lin Ma
Demin Li
Baoci Shan
Publication date
01-08-2018
Publisher
Springer US
Published in
Obesity Surgery / Issue 8/2018
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-018-3178-z

Other articles of this Issue 8/2018

Obesity Surgery 8/2018 Go to the issue