Homeostatic, reward and executive brain functions after gastric bypass surgery

Hankir, Mohammed K.; Al-Bas, Siham; Rullmann, Michael; Chakaroun, Rima; Seyfried, Florian; Pleger, Burkhard

doi:10.1016/j.appet.2019.104419

Cited by 17 publications

(10 citation statements)

References 99 publications

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“…The improvement in insulin sensitivity following surgery could also be an important mechanism to explain the changes in neural activity since brain insulin resistance has previously been associated with alterations in cerebral glucose metabolism, brain atrophy, and cognitive alterations (70,71). Other mechanisms have been proposed to explain the effects of bariatric surgery on brain structure and function, including the improvement of chronic low-grade inflammation, changes in incretin/gut peptide secretion (35,72) and microbiota products that impact the brain (33,73,74). A better understanding of the cellular/biological mechanisms through which the cardiometabolic changes following bariatric surgery influence human brain function and structure is of particular importance.…”

Section: Discussionmentioning

confidence: 99%

Spontaneous Neural Activity Changes after Bariatric Surgery: a resting-state fMRI study

Zeighami

Iceta

Dadar

et al. 2021

Preprint

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Background: Metabolic disorders associated with obesity could lead to alterations in brain structure and function. Whether these changes can be reversed after weight loss is unclear. Bariatric surgery provides a unique opportunity to address these questions because it induces marked weight loss and metabolic improvements which in turn may impact the brain in a longitudinal fashion. Previous studies found widespread changes in grey matter (GM) and white matter (WM) after bariatric surgery. However, findings regarding changes in spontaneous neural activity following surgery, as assessed with the fractional amplitude of low frequency fluctuations (fALFF) and regional homogeneity of neural activity (ReHo), are scarce and heterogenous. In this study, we used a longitudinal design to examine the changes in spontaneous neural activity after bariatric surgery (comparing pre- to post-surgery), and to determine whether these changes are related to cardiometabolic variables. Methods: The study included 57 participants with severe obesity who underwent sleeve gastrectomy (SG), biliopancreatic diversion with duodenal switch (BPD), or Roux-en-Y gastric bypass (RYGB), scanned prior to bariatric surgery and at follow-up visits of 4 months (N=36), 12 months (N=29), and 24 months (N=14) after surgery. We examined fALFF and ReHo measures across 1022 cortical and subcortical regions (based on combined Schaeffer-Xiao parcellations) using a linear mixed effect model. Voxel-based morphometry (VBM) based on T1-weighted images was also used to measure GM density in the same regions. We also used an independent sample from the Human Connectome Project (HCP) to assess regional differences between individuals who had normal-weight (N=46) or severe obesity (N=46). Results: We found a global increase in the fALFF signal with greater increase within dorsolateral prefrontal cortex, precuneus, inferior temporal gyrus, and visual cortex. This effect was more significant 4 months after surgery. The increase within dorsolateral prefrontal cortex, temporal gyrus, and visual cortex was more limited after 12 months and only present in the visual cortex after 24 months. These increases in neural activity measured by fALFF were also significantly associated with the increase in GM density following surgery. Furthermore, the increase in neural activity was significantly related to post-surgery weight loss and improvement in cardiometabolic variables, such as insulin resistance index and blood pressure. In the independent HCP sample, normal-weight participants had higher global and regional fALFF signals, mainly in dorsolateral/medial frontal cortex, precuneus and middle/inferior temporal gyrus compared to the obese participants. These BMI-related differences in fALFF were associated with the increase in fALFF 4 months post-surgery especially in regions involved in control, default mode and dorsal attention networks. Conclusions: Bariatric surgery-induced weight loss and improvement in metabolic factors are associated with widespread global and regional increases in neural activity, as measured by fALFF signal. These findings alongside the higher fALFF signal in normal-weight participants compared to participants with severe obesity in an independent dataset suggest an early recovery in the neural activity signal level after the surgery.

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Section: Discussionmentioning

confidence: 99%

Spontaneous Neural Activity Changes after Bariatric Surgery: a resting-state fMRI study

Zeighami

Iceta

Dadar

et al. 2021

Preprint

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“…Surgical therapy for weight loss has been discussed to convey more benefits to the patient than solely on the metabolic level, including neuroplasticity (45,46) . A considerable number of pre-to-post-surgery MRI analyses in relatively small sample sizes indeed indicated a certain recovery of structural and functional brain measures as well as cognitive performance after surgery [reviewed in (47) ], with the common limitation of lacking a longitudinal obese control group (see also Section 'Challenges of MRI in obesity and intervention studies'): for an in-depth review on bariatric surgery and weight loss mechanisms, see (48) .…”

Section: Obesity Surgerymentioning

confidence: 99%

Impact of obesity and diet on brain structure and function: a gut–brain–body crosstalk

Medawar

Witte

2022

Proc. Nutr. Soc.

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Most societies witness an ever increasing prevalence of both obesity and dementia, a scenario related to often underestimated individual and public health burden. Overnutrition and weight gain have been linked with abnormal functionality of homoeostasis brain networks and changes in higher cognitive functions such as reward evaluation, executive functions and learning and memory. In parallel, evidence has accumulated that modifiable factors such as obesity and diet impact the gut–brain axis and modulate brain health and cognition through various pathways. Using neuroimaging data from epidemiological studies and randomised clinical trials, we aim to shed light on the underlying mechanisms and to determine both determinants and consequences of obesity and diet at the level of human brain structure and function. We analysed multimodal 3T MRI of about 2600 randomly selected adults (47 % female, 18–80 years of age, BMI 18–47 kg/m2) of the LIFE-Adult study, a deeply phenotyped population-based cohort. In addition, brain MRI data of controlled intervention studies on weight loss and healthy diets acquired in lean, overweight and obese participants may help to understand the role of the gut–brain axis in food craving and cognitive ageing. We find that higher BMI and visceral fat accumulation correlate with accelerated brain age, microstructure of the hypothalamus, lower thickness and connectivity in default mode- and reward-related areas, as well as with subtle grey matter atrophy and white matter lesion load in non-demented individuals. Mediation analyses indicated that higher visceral fat affects brain tissue through systemic low-grade inflammation, and that obesity-related regional changes translate into cognitive disadvantages. Considering longitudinal studies, some, but not all data indicate beneficial effects of weight loss and healthy diets such as plant-based nutrients and dietary patterns on brain ageing and cognition. Confounding effects of concurrent changes in other lifestyle factors or false positives might help to explain these findings. Therefore a more holistic intervention approach, along with open science tools such as data and code sharing, in-depth pre-registration and pooling of data could help to overcome these limitations. In addition, as higher BMI relates to increased head micro-movements during MRI, and as head motion in turn systematically induces image artefacts, future studies need to rigorously control for head motion during MRI to enable valid neuroimaging results. In sum, our results support the view that overweight and obesity are intertwined with markers of brain health in the general population, and that weight loss and plant-based diets may help to promote brain plasticity. Meta-analyses and longitudinal cohort studies are underway to further differentiate causation from correlation in obesity- and nutrition-brain research.

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“…Hunger is thought to be driven more by homeostatic endocrine signaling mechanisms, while appetite is understood to be motivated more by hedonic reward pathways. Bariatric surgery may alter the hedonic or rewarding properties of food and that may contribute to changes in hunger, appetite, food preference, and actual consumption [9][10][11]. The decline in food intake following VSG may also result from the combination of food capacity restriction and alterations in circulating endocrine hormones in opposition to food intake [12,13].…”

Section: Introductionmentioning

confidence: 99%

Impact of Sleeve Gastrectomy on Subjective Hunger and Appetite Ratings and Endocrine Hormones

Leon

White

Casimiro

et al. 2022

Preprint

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Background: The effects of vertical sleeve gastrectomy (VSG) surgery on the levels of patients’ hunger and appetite across the day and relation to weight loss achieved were examined. Methods: Visual analog scale (VAS) hunger and appetite ratings were digitally collected from 10 female participants across a day during in-lab sessions 1-2 weeks before and 12 weeks after surgery. Fasting hormone levels were also assessed in 8 participants. Results: Post-surgery ratings were reduced overall despite fasting levels of leptin and ghrelin changing in favor of increased food intake. Notably, the majority of ratings from before breakfast were not different from ratings after dinner, suggesting that VSG induces changes that overcome the homeostatic drive to oppose a hypocaloric diet. Conclusions: These findings highlight the effectiveness of sleeve gastrectomy surgery in curbing food-seeking behavior despite a negative calorie balance.

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Homeostatic, reward and executive brain functions after gastric bypass surgery

Cited by 17 publications

References 99 publications

Spontaneous Neural Activity Changes after Bariatric Surgery: a resting-state fMRI study

Spontaneous Neural Activity Changes after Bariatric Surgery: a resting-state fMRI study

Impact of obesity and diet on brain structure and function: a gut–brain–body crosstalk

Impact of Sleeve Gastrectomy on Subjective Hunger and Appetite Ratings and Endocrine Hormones

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