Bariatric Surgery Induces White and Grey Matter Density Recovery in the Morbidly Obese: A Voxel‐Based Morphometric Study

Tuulari, Jetro J.; Karlsson, H.; Antikainen, Olli; Hirvonen, Jussi; Pham, Tam; Salminen, Paulina; Helmiö, Mika; Parkkola, Riitta; Nuutila, Pirjo; Nummenmaa, Lauri

doi:10.1002/hbm.23272

Cited by 82 publications

(72 citation statements)

References 44 publications

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“…Imaging studies in humans previously reported that obese individuals have reduced WM tissue density and altered WM integrity in dispersed tracts, including the corpus callosum, cingulum, cerebellar peduncle and corona radiata (9,12,13,17,19,29,43). These findings align well with our cross-sectional results showing that WM density in brain stem and cerebellar peduncle, two regions that significantly increased after SG, were reduced in severely obese individuals compared to normal-weight individuals.…”

Section: Discussionsupporting

confidence: 91%

“…As previously reported by other groups (9,29), we observed that bariatric surgery-induced weight loss was associated with increased global WM density, particularly in the cerebellum, brain stem, cerebellar peduncle, cingulum, corpus callosum and corona radiata.…”

Section: Discussionsupporting

confidence: 88%

“…For instance, our recent neuroimaging coordinate-based meta-analysis on voxel-based morphometry (VBM) demonstrated that obesity is associated with reduced GM volume in discrete brain regions, namely the ventromedial prefrontal cortex, cerebellum and portions of temporal and parietal lobes (8). A study in morbidly obese participants undergoing bariatric surgery found widespread cortical and subcortical GM atrophy prior to surgery (9). In a cross-sectional study, obesity was also associated with a greater degree of WM atrophy, with an estimated increase in brain age of 10 years (10).…”

Section: Introductionmentioning

confidence: 99%

“…Growing evidence shows improvement in cognitive functions after bariatric surgery (26,27). However, only few structural MRI studies examined changes in GM and WM densities after bariatric surgery (9,28,29). Tuulari et al (9) were the first to show global increase in WM density and limited increase in GM density (occipital and temporal regions) 6 months after bariatric surgery using VBM.…”

Section: Introductionmentioning

confidence: 99%

“…However, only few structural MRI studies examined changes in GM and WM densities after bariatric surgery (9,28,29). Tuulari et al (9) were the first to show global increase in WM density and limited increase in GM density (occipital and temporal regions) 6 months after bariatric surgery using VBM. Zhang et al (29) observed increased GM and WM densities as well as improved WM integrity in regions involved in food intake control and cognitiveemotion regulation 1 month following sleeve gastrectomy (SG) compared to baseline.…”

Section: Introductionmentioning

confidence: 99%

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Neuroanatomical Changes in White and Grey Matter after Sleeve Gastrectomy

Michaud

Dadar

Pelletier

et al. 2019

Preprint

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Background: MRI studies show that obese adults have reduced grey (GM) and white matter (WM) tissue density as well as altered WM integrity. It remains to be examined if bariatric surgery induces structural brain changes. The aim of this study is to characterize GM and WM density changes in a longitudinal setting, comparing pre-and post-operation and to determine whether these changes are related to inflammation and cardiometabolic markers. Methods: 29 severely obese participants (age: 45.9±7.8 years) scheduled to undergo sleeve gastrectomy (SG) were recruited. High-resolution T1-weighted anatomical images were acquired 1 month prior to as well as 4 and 12 months after surgery. GM and WM densities were quantified using voxel-based morphometry (VBM). Circulating lipid profile, glucose, insulin and inflammatory markers (interleukin (IL)-6, C-reactive protein (CRP) and lipopolysaccharide-binding protein (LBP) were measured at each time point.A linear mixed effect model was used to compare brain changes before and after SG, controlling for age, gender, initial BMI and diabetic status. To assess the associations between changes in adiposity, metabolism and inflammation and changes in GM or WM density, the mean GM and WM densities were extracted across all the participants using atlas, and linear mixed-effect models were used. Results: As expected, weight, BMI, waist circumference and neck circumference significantly decreased after SG compared with baseline (p<0.001 for all). A widespread increase in WM density was observed after surgery, particularly in the cerebellum, brain stem, cerebellar peduncle, cingulum, corpus callosum and corona radiata (p<0.05, after FDR correction). Significant increases in GM density were observed 4 months after SG compared to baseline in several brain regions such as the bilateral occipital cortex, temporal cortex, precentral gyrus and cerebellum as Michaud et al. 2019, page 3 well as right fusiform gyrus, right hippocampus and right insula. These GM and WM increases were more pronounced and widespread after 12 months and were significantly associated with post-operative weight loss and the improvement of metabolic alterations.Our linear mixed-effect models also showed strong associations between post-operative reductions in LBP, a marker of inflammation, and increased WM density. To confirm our results, we tested whether the peak of each significant region showed BMI-related differences in an independent dataset (Human Connectome Project). We matched a group of severely obese individuals with a group of lean individuals for age, gender and ethnicity.Severe obesity was associated with reduced WM density in the brain stem and cerebellar peduncle as well as reduced GM density in cerebellum, regions that significantly changed after surgery (p<0.01 for all clusters). Conclusions: Bariatric surgery-induced weight loss and improvement in metabolic alterations is associated with widespread increases in WM and GM densities. These post-operative changes overlapped with baseline brain difference...

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Neuroanatomical Changes in White and Grey Matter after Sleeve Gastrectomy

Michaud

Dadar

Pelletier

et al. 2019

Preprint

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Associations Between Socioeconomic Status, Obesity, Cognition, and White Matter Microstructure in Children

Cai

Taylor

et al. 2023

JAMA Netw Open

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ImportanceLower neighborhood and household socioeconomic status (SES) are associated with negative health outcomes and altered brain structure in children. It is unclear whether such findings extend to white matter and via what mechanisms.ObjectiveTo assess whether and how neighborhood and household SES are independently associated with children’s white matter microstructure and examine whether obesity and cognitive performance (reflecting environmental cognitive and sensory stimulation) are plausible mediators.Design, Setting, and ParticipantsThis cross-sectional study used baseline data from participants in the Adolescent Brain Cognitive Development (ABCD) study. Data were collected at 21 US sites, and school-based recruitment was used to represent the US population. Children aged 9 to 11 years and their parents or caregivers completed assessments between October 1, 2016, and October 31, 2018. After exclusions, 8842 of 11 875 children in the ABCD study were included in the analyses. Data analysis was conducted from July 11 to December 19, 2022.ExposuresNeighborhood disadvantage was derived from area deprivation indices at participants’ primary residence. Household SES factors were total income and highest parental educational attainment.Main Outcomes and MeasuresA restriction spectrum imaging (RSI) model was used to quantify restricted normalized directional (RND; reflecting oriented myelin organization) and restricted normalized isotropic (RNI; reflecting glial and neuronal cell bodies) diffusion in 31 major white matter tracts. The RSI measurements were scanner harmonized. Obesity was assessed through body mass index (BMI; calculated as weight in kilograms divided by height in meters squared), age- and sex-adjusted BMI z scores, and waist circumference, and cognition was assessed through the National Institutes of Health Toolbox Cognition Battery. Analyses were adjusted for age, sex, pubertal development stage, intracranial volume, mean head motion, and twin or siblingship.ResultsAmong 8842 children, 4543 (51.4%) were boys, and the mean (SD) age was 9.9 (0.7) years. Linear mixed-effects models revealed that greater neighborhood disadvantage was associated with lower RSI-RND in the left superior longitudinal fasciculus (β = −0.055; 95% CI, −0.081 to −0.028) and forceps major (β = −0.040; 95% CI, −0.067 to −0.013). Lower parental educational attainment was associated with lower RSI-RND in the bilateral superior longitudinal fasciculus (eg, right hemisphere: β = 0.053; 95% CI, 0.025-0.080) and bilateral corticospinal or pyramidal tract (eg, right hemisphere: β = 0.042; 95% CI, 0.015-0.069). Structural equation models revealed that lower cognitive performance (eg, lower total cognition score and higher neighborhood disadvantage: β = −0.012; 95% CI, −0.016 to −0.009) and greater obesity (eg, higher BMI and higher neighborhood disadvantage: β = −0.004; 95% CI, −0.006 to −0.001) partially accounted for the associations between SES and RSI-RND. Lower household income was associated with higher RSI-RNI in most tracts (eg, right inferior longitudinal fasciculus: β = −0.042 [95% CI, −0.073 to −0.012]; right anterior thalamic radiations: β = −0.045 [95% CI, −0.075 to −0.014]), and greater neighborhood disadvantage had similar associations in primarily frontolimbic tracts (eg, right fornix: β = 0.046 [95% CI, 0.019-0.074]; right anterior thalamic radiations: β = 0.045 [95% CI, 0.018-0.072]). Lower parental educational attainment was associated with higher RSI-RNI in the forceps major (β = −0.048; 95% CI, −0.077 to −0.020). Greater obesity partially accounted for these SES associations with RSI-RNI (eg, higher BMI and higher neighborhood disadvantage: β = 0.015; 95% CI, 0.011-0.020). Findings were robust in sensitivity analyses and were corroborated using diffusion tensor imaging.Conclusions and RelevanceIn this cross-sectional study, both neighborhood and household contexts were associated with white matter development in children, and findings suggested that obesity and cognitive performance were possible mediators in these associations. Future research on children’s brain health may benefit from considering these factors from multiple socioeconomic perspectives.

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Long-Term Brain Structure and Cognition Following Bariatric Surgery

Custers,

Vreeken,

Kleemann

et al. 2024

JAMA Netw Open

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ImportanceWeight loss induced by bariatric surgery (BS) is associated with improved cognition and changed brain structure; however, previous studies on the association have used small cohorts and short follow-up periods, making it difficult to determine long-term neurological outcomes associated with BS.ObjectiveTo investigate long-term associations of weight loss after BS with cognition and brain structure and perfusion.Design, Setting, and ParticipantsThis cohort study included participants from the Bariatric Surgery Rijnstate and Radboudumc Neuroimaging and Cognition in Obesity study. Data from participants with severe obesity (body mass index [BMI; calculated as weight in kilograms divided by height in meters squared] &gt;40, or BMI &gt;35 with comorbidities) eligible for Roux-en-Y gastric bypass and aged 35 to 55 years were enrolled from a hospital specialized in BS (Rijnstate Hospital, Arnhem, the Netherlands). Participants were recruited between September 2018 and December 2020 with follow-up till March 2023. Data were collected before BS and at 6 and 24 months after BS. Data were analyzed from March to November 2023.ExposureRoux-en-Y gastric bypass.Main Outcomes and MeasuresPrimary outcomes included body weight, BMI, waist circumference, blood pressure, medication use, cognitive performance (20% change index of compound z-score), brain volumes, cortical thickness, cerebral blood flow (CBF), and spatial coefficient of variation (sCOV). Secondary outcomes include cytokines, adipokines, depressive symptoms (assessed using the Beck Depression Inventory), and physical activity (assessed using the Baecke Questionnaire).ResultsA total of 133 participants (mean [SD] age, 46.8 [5.7] years; 112 [84.2%] female) were included. Global cognition was at least 20% higher in 52 participants (42.9%) at 24 months after BS. Compared with baseline, at 24 months, inflammatory markers were lower (mean [SD] high-sensitivity C-reactive protein: 4.77 [5.80] μg/mL vs 0.80 [1.09] μg/mL; P &lt; .001), fewer patients used antihypertensives (48 patients [36.1%] vs 22 patients [16.7%]), and patients had lower depressive symptoms (median [IQR] BDI score: 9.0 [5.0-13.0] vs 3.0 [1.0-6.0]; P &lt; .001) and greater physical activity (mean [SD] Baecke score: 7.64 [1.29] vs 8.19 [1.35]; P &lt; .001). After BS, brain structure and perfusion were lower in most brain regions, while hippocampal and white matter volume remained stable. CBF and sCOV did not change in nucleus accumbens and parietal cortex. The temporal cortex showed a greater thickness (mean [SD] thickness: 2.724 [0.101] mm vs 2.761 [0.007] mm; P = .007) and lower sCOV (median [IQR] sCOV: 4.41% [3.83%-5.18%] vs 3.97% [3.71%-4.59%]; P = .02) after BS.Conclusions and RelevanceThese findings suggest that BS was associated with health benefits 2 years after surgery. BS was associated with improved cognition and general health and changed blood vessel efficiency and cortical thickness of the temporal cortex. These results may improve treatment options for patients with obesity and dementia.

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Bariatric Surgery Induces White and Grey Matter Density Recovery in the Morbidly Obese: A Voxel‐Based Morphometric Study

Cited by 82 publications

References 44 publications

Neuroanatomical Changes in White and Grey Matter after Sleeve Gastrectomy

Neuroanatomical Changes in White and Grey Matter after Sleeve Gastrectomy

Associations Between Socioeconomic Status, Obesity, Cognition, and White Matter Microstructure in Children

Long-Term Brain Structure and Cognition Following Bariatric Surgery

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