Previous studies suggest that obesity (OB) is associated with disrupted brain network organization; however, it remains unclear whether these differences already exist during childhood. Moreover, it should be investigated whether deviant network organization may be susceptible to treatment.
Here, we compared the structural connectomes of children with OB with age-matched healthy weight (HW) controls (aged 7–11 years). In addition, we examined the effect of a multidisciplinary treatment program, consisting of diet restriction, cognitive behavioral therapy, and physical activity for children with OB on brain network organization. After stringent quality assessment criteria, 40 (18 OB, 22 HW) data sets of the total sample of 51 participants (25 OB, 26 HW) were included in further analyses. For all participants, anthropometric measurements were administered twice, with a 5-month interval between pre- and post tests. Pre- and post T1- and diffusion-weighted imaging scans were also acquired and analyzed using a graph-theoretical approach and network-based statistics.
Global network analyses revealed a significantly increased normalized clustering coefficient and small-worldness in children with OB compared with HW controls. In addition, regional analyses revealed increased betweenness centrality, reduced clustering coefficient, and increased structural network strength in children with OB, mainly in the motor cortex and reward network. Importantly, children with OB lost a considerable amount of their body mass after the treatment; however, no changes were observed in the organization of their brain networks.
This is the first study showing disrupted structural connectomes of children with OB, especially in the motor and reward network. These results provide new insights into the pathophysiology underlying childhood obesity. The treatment did result in a significant weight loss, which was however not associated with alterations in the brain networks. These findings call for larger samples to examine the impact of short-term and long-term weight loss (treatment) on children’s brain network organization.
Access optionsAccess options
Subscribe to Journal
Get full journal access for 1 year
only $64.42 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Sahoo K, Sahoo B, Choudhury AK, Sufi NY, Kumar R, Bhadoria AS. Childhood obesity: causes and consequences. J Fam Med Prim Care. 2015;4:187–92.
Keating CL, Moodie ML, Swinburn BA. The health-related quality of life of overweight and obese adolescents – a study measuring body mass index and adolescent-reported perceptions. Int J Pediatr Obes. 2011;6:434–41.
Wijnhoven TM, van Raaij JM, Yngve A, Sjöberg A, Kunešová M, Duleva V, et al. WHO European Childhood Obesity Surveillance Initiative: health-risk behaviours on nutrition and physical activity in 6–9-year-old school children. Public Health Nutr. 2015;18:3108–24.
Robinson LE, Stodden DF, Barnett LM, Lopes VP, Logan SW, Rodrigues LP, et al. Motor competence and its effect on positive developmental trajectories of health. Sport Med. 2015;45:1273–84.
Joseph RJ, Alonso-Alonso M, Bond DS, Pascual-Leone A, Blackburn GL. The neurocognitive connection between physical activity and eating behaviour. Obes Rev. 2011;12:800–12.
Liang J, Matheson BE, Kaye WH, Boutelle KN. Neurocognitive correlates of obesity and obesity-related behaviors in children and adolescents. Int J Obes. 2014;38:494–506.
Hansen CJ, Stevens LC, Coast JR. Exercise duration and mood state: how much is enough to feel better? Heal Psychol. 2001;20:267–75.
Ou X, Andres A, Pivik RT, Cleves MA, Badger TM. Brain gray and white matter differences in healthy normal weight and obese children. J Magn Reson Imaging. 2015;42:1205–13.
Moreno-López L, Soriano-Mas C, Delgado-Rico E, Rio-Valle JS, Verdejo-García A. Brain structural correlates of reward sensitivity and impulsivity in adolescents with normal and excess weight. PLoS ONE. 2012;7:e49185.
Augustijn MJCM, Deconinck FJA, D’Hondt E, Van Acker L, De Guchtenaere A, Lenoir M, et al. Reduced motor competence in children with obesity is associated with structural differences in the cerebellar peduncles. Brain Imaging Behav. 2018;12:1000–10.
MJCM Augustijn, D’Hondt E, Leemans A, Van Acker L, De Guchtenaere A, Lenoir M, et al. Weight loss, behavioural change and structural neuroplasticity in children with obesity through a multidisciplinary treatment program. Hum Brain Mapp. 2018;12:1000–10.
Bressler SL, Menon V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci. 2010;14:277–90.
Rubinov M, Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage. 2010;52:1059–69.
Bassett DS, Bullmore E. Small-world brain networks. Neuroscientist. 2006;12:512–23.
Bruce AS, Martin LE, Savage CR. Neural correlates of pediatric obesity. Prev Med. 2011;52:S29–35.
Sporns O, Tononi G, Kötter R. The human connectome: a structural description of the human brain. PLoS Comput Biol. 2005;1:0245–51.
Griffa A, Baumann PS, Thiran JP, Hagmann P. Structural connectomics in brain diseases. Neuroimage. 2013;80:515–26.
Chao S-H, Liao Y-T, Chen VC-H, Li C-J, McIntyre RS, Lee Y, et al. Correlation between brain circuit segregation and obesity. Behav Brain Res. 2018;337:218–27.
Baek K, Morris LS, Kundu P, Voon V. Disrupted resting-state brain network properties in obesity: decreased global and putaminal cortico-striatal network efficiency. Psychol Med. 2017;47:585–96.
Marqués-Iturria I, Scholtens LH, Garolera M, Pueyo R, García-García I, González-Tartiere P, et al. Affected connectivity organization of the reward system structure in obesity. Neuroimage. 2015;111:100–6.
Yuan W, Treble-Barna A, Sohlberg MM, Harn B, Wade SL. Changes in structural connectivity following a cognitive intervention in children with traumatic brain injury. Neurorehabil Neural Repair. 2017;31:190–201.
Yuan W, Wade SL, Quatman-Yates C, Hugentobler JA, Gubanich PJ, Kurowski BG. Structural connectivity related to persistent symptoms after mild tbi in adolescents and response to aerobic training: preliminary investigation. J Head Trauma Rehabil. 2017;32:378–84.
Amidi A, Hosseini SMH, Leemans A, Kesler SR, Agerbæk M, Wu LM, et al. Changes in brain structural networks and cognitive functions in testicular cancer patients receiving cisplatin-based chemotherapy. J Natl Cancer Inst. 2017;109:1–7.
Langer N, von Bastian CC, Wirz H, Oberauer K, Jäncke L. The effects of working memory training on functional brain network efficiency. Cortex. 2013;49:2424–38.
Caeyenberghs K, Metzler-Baddeley C, Foley S, Jones DK. Dynamics of the human structural connectome underlying working memory training. J Neurosci. 2016;36:4056–66.
Zalesky A, Fornito A, Bullmore ET. Network-based statistic: identifying differences in brain networks. Neuroimage. 2010;53:1197–207.
Cole TJ, Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatr Obes. 2012;7:284–94.
D’Hondt E, Gentier I, Deforche B, Tanghe A, De Bourdeaudhuij I, Lenoir M. Weight loss and improved gross motor coordination in children as a result of multidisciplinary residential obesity treatment. Obesity. 2011;19:1999–2005.
Gentier I, D’Hondt E, Augustijn M, Tanghe A, De Bourdeaudhuij I, Deforche B, et al. Multidisciplinary residential treatment can improve perceptual-motor function in obese children. Acta Paediatr. 2015;104:e263–70.
Goscinski WJ, McIntosh P, Felzmann U, Maksimenko A, Hall CJ, Gureyev T, et al. The Multi-modal Australian ScienceS Imaging and Visualization Environment (MASSIVE) high performance computing infrastructure: applications in neuroscience and neuroinformatics research. Front Neuroinform. 2014;8:1–13.
Roberts JA, Perry A, Lord AR, Roberts G, Mitchell PB, Smith RE, et al. The contribution of geometry to the human connectome. Neuroimage. 2016;124:379–93.
Zalesky A, Fornito A, Cocchi L, Gollo LL, van den Heuvel MP, Breakspear M. Connectome sensitivity or specificity: which is more important? Neuroimage. 2016;142:407–20.
Kaiser M, Hilgetag CC. Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol. 2006;2:0805–15.
Hosseini SMH, Hoeft F, Kesler SR, Lambiotte R. GAT: a graph-theoretical analysis toolbox for analyzing between-group differences in large-scale structural and functional brain networks. PLoS ONE. 2012;7:e40709.
De Reus MA, Van Den Heuvel MP. Estimating false positives and negatives in brain networks. Neuroimage. 2013;70:402–9.
Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970;45:13–23.
Caeyenberghs K, Clemente A, Imms P, Egan G, Hocking DR, Leemans A, et al. Evidence for training-dependent structural neuroplasticity in brain-injured patients: a critical review. Neurorehabil Neural Repair. 2018;32:99–114.
Hagmann P, Sporns O, Madan N, Cammoun L, Pienaar R, Wedeen VJ, et al. White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci USA. 2010;107:19067–72.
Collin G, Van Den, Heuvel MP. The ontogeny of the human connectome: Development and dynamic changes of brain connectivity across the life span. Neuroscientist. 2013;19:616–28.
Fair DA, Cohen AL, Power JD, Dosenbach NUF, Church JA, Miezin FM, et al. Functional brain networks develop from a “Local to Distributed” organization. PLoS Comput Biol. 2009;5:e1000381.
Wang L, Zhu C, He Y, Zang Y, Cao Q, Zhang H, et al. Altered small-world brain functional networks in children with attention-deficit/hyperactivity disorder. Hum Brain Mapp. 2009;30:638–49.
Di Martino A, Fair DA, Kelly C, Satterthwaite TD, Castellanos FX, Thomason ME, et al. Unraveling the miswired connectome: a developmental perspective. Neuron. 2014;83:1335–53.
Caeyenberghs K, Taymans T, Wilson PH, Vanderstraeten G, Hosseini H, van Waelvelde H. Neural signature of developmental coordination disorder in the structural connectome independent of comorbid autism. Dev Sci. 2016;19:599–612.
Rizzolatti G, Luppino G. The cortical motor system. Neuron. 2001;31:889–901.
D’Hondt E, Deforche B, De Bourdeaudhuij I, Lenoir M. Childhood obesity affects fine motor skill performance under different postural constraints. Neurosci Lett. 2008;440:72–5.
D’Hondt E, Deforche B, De Bourdeaudhuij I, Lenoir M. Relationship between motor skill and body mass index in 5- to 10-year-old children. Adapt Phys Activ Q. 2009;26:21–37.
Gentier I, D’Hondt E, Shultz S, Deforche B, Augustijn M, Hoorne S, et al. Fine and gross motor skills differ between healthy-weight and obese children. Res Dev Disabil. 2013;34:4043–51.
Sporns O, Honey CJ, Kötter R. Identification and classification of hubs in brain networks. PLoS ONE. 2007;2:e1049.
Rudebeck PH, Murray EA. The orbitofrontal oracle: cortical mechanisms for the prediction and evaluation of specific behavioral outcomes. Neuron. 2014;84:1143–56.
Volkow ND, Wang G-J, Baler RD. Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci. 2011;15:37–46.
van den Berg L, Pieterse K, Malik JA, Luman M, Willems van Dijk K, Oosterlaan J, et al. Association between impulsivity, reward responsiveness and body mass index in children. Int J Obes. 2011;35:1301–7.
Verdejo-García A, Verdejo-Román J, Rio-Valle JS, Lacomba JA, Lagos FM, Soriano-Mas C. Dysfunctional involvement of emotion and reward brain regions on social decision making in excess weight adolescents. Hum Brain Mapp. 2015;36:226–37.
Kravitz AV, O’Neal TJ, Friend DM. Do dopaminergic impairments underlie physical inactivity in people with obesity? Front Hum Neurosci. 2016;10:1–8. (514)
Diamond A. Executive functions. Annu Rev Psychol. 2013;64:135–68.
Casey BJ, Giedd JN, Thomas KM. Structural and functional brain development and its relation to cognitive development. Biol Psychol. 2000;54:241–57.
Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis a C, et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA. 2004;101:8174–9.
Willoughby T, Good M, Adachi PJC, Hamza C, Tavernier R. Examining the link between adolescent brain development and risk taking from a social-developmental perspective. Brain Cogn. 2014;89:70–8.
Deforche B, De Bourdeaudhuij I, Debode P, Vinaimont F, Hills AP, Verstraete S, et al. Changes in fat mass, fat-free mass and aerobic fitness in severely obese children and adolescents following a residential treatment programme. Eur J Pediatr. 2003;162:616–22.
Braet C, Tanghe A, Decaluwé V, Moens E, Rosseel Y. Inpatient treatment for children with obesity: weight loss, psychological well-being, and eating behavior. J Pediatr Psychol. 2004;29:519–29.
Weise CM, Thiyyagura P, Reiman EM, Chen K, Krakoff J. 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.
Thomas C, Baker CI. Teaching an adult brain new tricks: a critical review of evidence for training-dependent structural plasticity in humans. Neuroimage. 2013;73:225–36.
Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage. 2012;62:782–90.
Tournier J-DD, Calamante F, Connelly A. MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol. 2012;22:53–66.
Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968–80.
The study was funded by the Ph.D. fellowship of the Research Foundation Flanders (FWO) awarded to MJCMA [3F000714]. The authors are very grateful to all participants and their parents, the staff from the rehabilitation center “Zeepreventorium” (De Haan, Belgium), and the board of the participating schools.
This study was funded by the Ph.D. fellowship of the Research Foundation Flanders (FWO) awarded to MJCMA [3F000714].
Conflict of interest
The authors declare that they have no conflict of interest.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.