Abstract
Obesity is often associated with cardiovascular complications. Adolescent obesity is a risk factor for cardiovascular disease in adulthood; thus, intensive management is warranted in adolescence. The brain state contributes to the development of obesity in addition to metabolic conditions, and hence neuroimaging is an important tool for accurately assessing an individual’s risk of developing obesity. Here, we aimed to predict body mass index (BMI) progression in adolescents with neuroimaging features using machine learning approaches. From an open database, we adopted 76 resting-state functional magnetic resonance imaging (rs-fMRI) datasets from adolescents with longitudinal BMI scores. Functional connectivity analyses were performed on cortical surfaces and subcortical volumes. We identified baseline functional connectivity features in the prefrontal-, posterior cingulate-, sensorimotor-, and inferior parietal-cortices as significant determinants of BMI changes. A BMI prediction model based on the identified fMRI biomarkers exhibited a high accuracy (intra-class correlation = 0.98) in predicting BMI at the second visit (1~2 years later). The identified brain regions were significantly correlated with the eating disorder-, anxiety-, and depression-related scores. Based on these results, we concluded that these functional connectivity features in brain regions related to eating disorders and emotional processing could be important neuroimaging biomarkers for predicting BMI progression.
Similar content being viewed by others
Data availability
The imaging and phenotypic data are available from the Enhanced NKI-RS repository (http://fcon_1000.projects.nitrc.org/indi/enhanced/index.html). Interested researchers should contact the database administrator to request access to the data.
References
Anticevic, A., Dierker, D. L., Gillespie, S. K., Repovs, G., Csernansky, J. G., Van Essen, D. C., & Barch, D. M. (2008). Comparing surface-based and volume-based analyses of functional neuroimaging data in patients with schizophrenia. NeuroImage, 41(3), 835–848. https://doi.org/10.1016/j.neuroimage.2008.02.052.
Beckmann, C. F., & Smith, S. M. (2004). Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Transactions on Medical Imaging, 23, 137–152.
Beckmann, C. F., DeLuca, M., Devlin, J. T., & Smith, S. M. (2005). Investigations into resting-state connectivity using independent component analysis. Philosophical Transactions of the Royal Society B, 360(1457), 1001–1013. https://doi.org/10.1098/rstb.2005.1634.
Bohon, C. (2017). Brain response to taste in overweight children: A pilot feasibility study. PLoS One, 12(2), e0172604. https://doi.org/10.1371/journal.pone.0172604.
Brownell, K. D., & Wadden, T. A. (1991). The heterogeneity of obesity: Fitting treatments to individuals. Behavior Therapy, 22, 153–177. https://doi.org/10.1016/j.beth.2016.11.009.
Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The Brain’s default network: Anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124(1), 1–38. https://doi.org/10.1196/annals.1440.011.
Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Neuroscience, 10(3), 186–198. https://doi.org/10.1038/nrn2575.
Cerf-Ducastel, B., Van de Moortele, P. F., MacLeod, P., Le Bihan, D., & Faurion, A. (2001). Interaction of gustatory and lingual somatosensory perceptions at the cortical level in the human: a functional magnetic resonance imaging study. Chemical Senses, 26, 371–383. https://doi.org/10.1093/chemse/26.4.371.
Chan, R. C. K., Shum, D., Toulopoulou, T., & Chen, E. Y. H. (2008). Assessment of executive functions: Review of instruments and identification of critical issues. Archives of Clinical Neuropsychology, 23, 201–216. https://doi.org/10.1016/j.acn.2007.08.010.
Coalson, T. S., Van Essen, D. C., & Glasser, M. F. (2018). The impact of traditional neuroimaging methods on the spatial localization of cortical areas. Proceedings of the National Academy of Sciences, 115(27), E6356–E6365. https://doi.org/10.1073/pnas.1801582115.
Cornier, M. A., Salzberg, A. K., Endly, D. C., Bessesen, D. H., Rojas, D. C., & Tregellas, J. R. (2009). The effects of overfeeding on the neuronal response to visual food cues in thin and reduced-obese individuals. PLoS One, 4(7), e6310. https://doi.org/10.1371/journal.pone.0006310.
Cox, R. W. (1996). AFNI : Software for analysis and visualization of functional magnetic resonance Neuroimages. Computers and Biomedical Research, 29, 162–173. https://doi.org/10.1006/cbmr.1996.0014.
Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis: I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194. https://doi.org/10.1006/nimg.1998.0395.
Davids, S., Lauffer, H., Thoms, K., Jagdhuhn, M., Hirschfeld, H., Domin, M., Hamm, A., & Lotze, M. (2010). Increased dorsolateral prefrontal cortex activation in obese children during observation of food stimuli. International Journal of Obesity, 34(1), 94–104. https://doi.org/10.1038/ijo.2009.193.
DelParigi, A., Chen, K., Salbe, A. D., Reiman, E. M., & Tataranni, P. A. (2005). Sensory experience of food and obesity: a positron emission tomography study of the brain regions affected by tasting a liquid meal after a prolonged fast. NeuroImage, 24(2), 436–443. https://doi.org/10.1016/j.neuroimage.2004.08.035.
Engelen, T., de Graaf, T. A., Sack, A. T., & de Gelder, B. (2015). A causal role for inferior parietal lobule in emotion body perception. Cortex, 73, 195–202. https://doi.org/10.1016/j.cortex.2015.08.013.
Fairburn, C., & Beglin, S. (1994). Assessment of eating disorders: Interview or self- report questionnaire? International Journal of Eating Disorders, 16(4), 363–370. https://doi.org/10.1002/1098-108X(199412)16:4<363::AID-EAT2260160405>3.0.CO;2-#.
Fischl, B. (2012). FreeSurfer. NeuroImage, 62(2), 774–781. https://doi.org/10.1016/j.neuroimage.2012.01.021.
Fischl, B., Sereno, M. I., & Dale, A. M. (1999a). Cortical surface-based analysis: II. Inflation, flattening, and a surface-based coordinate system. NeuroImage, 9(2), 195–207. https://doi.org/10.1006/nimg.1998.0396.
Fischl, B., Sereno, M. I., Tootell, R. B. H., & Dale, A. M. (1999b). High-resolution inter-subject averaging and a surface-based coordinate system. Human Brain Mapping, 8, 272–284. https://doi.org/10.1002/(SICI)1097-0193(1999)8.
Fischl, B., Liu, A., & Dale, A. M. (2001). Automated manifold surgery: Constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Transactions on Medical Imaging, 20(1), 70–80. https://doi.org/10.1109/42.906426.
Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., van der Kouwe, A., Killiany, R., Kennedy, D., Klaveness, S., Montillo, A., Makris, N., Rosen, B., & Dale, A. M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341–355. https://doi.org/10.1016/S0896-6273(02)00569-X.
Glasser, M. F., Sotiropoulos, S. N., Wilson, J. A., Coalson, T. S., Fischl, B., Andersson, J. L., Xu J., Jbabdi S., Webster M., Polimeni J.R., van Essen D., Jenkinson M., WU-Minn HCP Consortium. (2013). The minimal preprocessing pipelines for the human connectome project. NeuroImage, 80, 105–124. https://doi.org/10.1016/j.neuroimage.2013.04.127.
Glasser, M. F., Coalson, T. S., Robinson, E. C., Hacker, C. D., Harwell, J., Yacoub, E., Ugurbil, K., Andersson, J., Beckmann, C. F., Jenkinson, M., Smith, S. M., & van Essen, D. C. (2016). A multi-modal parcellation of human cerebral cortex. Nature, 536(7615), 171–178. https://doi.org/10.1038/nature18933.
Gunnell, D. J., Frankel, S. J., Nanchahal, K., Peters, T. J., & Smith, G. D. (1998). Childhood obesity and adult cardiovascular mortality: a 57-year follow-up study based on the Boyd Orr cohort. American Journal of Clinical Nutrition, 136, 664–672.
Guo, S. S., Wu, W., Chumlea, W. C., & Roche, A. F. (2002). Predicting overweight and obesity in adulthood from body mass index values in childhood and adolescence. The American Journal od Clinical Nutrition, 76, 653–658.
Harrison, R. N. S., Gaughran, F., Murray, R. M., Lee, S. H., Cano, J. P., Dempster, D., Curtis, C. J., Dima, D., Patel, H., de Jong, S., & Breen, G. (2017). Development of multivariable models to predict change in body mass index within a clinical trial population of psychotic individuals. Scientific Reports, 7, 14738. https://doi.org/10.1038/s41598-017-15137-7.
Ihmels, M. A., Welk, G. J., Eisenmann, J. C., Nusser, S. M., & Myers, E. F. (2009). Prediction of BMI change in young children with the family nutrition and physical activity (FNPA) screening tool. Annals of Behavioral Medicine, 38(1), 60–68. https://doi.org/10.1007/s12160-009-9126-3.
Jagust, W., Harvey, D., Mungas, D., & Haan, M. (2005). Central obesity and the aging brain. Archives of Neurology, 62(10), 1545–1548. https://doi.org/10.1001/archneur.62.10.1545.
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W., & Smith, S. M. (2012). FSL. Fsl. NeuroImage, 62(2), 782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015.
Jo, H. J., Lee, J. M., Kim, J. H., Shin, Y. W., Kim, I. Y., Kwon, J. S., & Kim, S. I. (2007). Spatial accuracy of fMRI activation influenced by volume- and surface-based spatial smoothing techniques. NeuroImage, 34(2), 550–564. https://doi.org/10.1016/j.neuroimage.2006.09.047.
Kamijo, K., Pontifex, M. B., Khan, N. A., Raine, L. B., Scudder, M. R., Drollette, E. S., Evans, E. M., Castelli, D. M., & Hillman, C. H. (2014). The negative association of childhood obesity to cognitive control of action monitoring. Cerebral Cortex, 24(3), 654–662. https://doi.org/10.1093/cercor/bhs349.
Kindblom, J. M., Lorentzon, M., Hellqvist, Å., Lo, L., Brandberg, J., Lönn, L., et al. (2009). BMI changes during childhood and adolescence as predictors of amount of adult subcutaneous and visceral adipose tissue in men. Diabetes, 58, 867–874. https://doi.org/10.2337/db08-0606.
Kovacs, M. (2011). Children’s depression inventory (2nd ed.). Toronto, Canada: Multi-Health Systems.
Kullmann, S., Heni, M., Veit, R., Ketterer, C., Schick, F., Häring, H. U., Fritsche, A., & Preissl, H. (2012). The obese brain: Association of body mass index and insulin sensitivity with resting state network functional connectivity. Human Brain Mapping, 33(5), 1052–1061. https://doi.org/10.1002/hbm.21268.
Laitinen, J., Power, C., & Järvelin, M.-R. (2001). Family social class, maternal body mass index, childhood body mass index, and age at menarche as predictors of adult obesity. The American Journal od Clinical Nutrition, 74(3), 287–294.
Le, D. S. N. T., Pannacciulli, N., Chen, K., Salbe, A. D., Hill, J. O., Wing, R. R., et al. (2007). Less activation in the left dorsolateral prefrontal cortex in the reanalysis of the response to a meal in obese than in lean women and its association with successful weight loss. American Journal of Clinical Nutrition, 86(3), 573–579.
Lips, M. a., Wijngaarden, M. a., Van Der Grond, J., Van Buchem, M. a., De Groot, G. H., Rombouts, S. a R. B., et al. (2014). Resting-state functional connectivity of brain regions involved in cognitive control, motivation, and reward is enhanced in obese females. American Journal of Clinical Nutrition, 100(2), 524–531. https://doi.org/10.3945/ajcn.113.080671.
Luppino, F. S., de Wit, L. M., Bouvy, P. F., Stijnen, T., Cuijpers, P., Penninx, B. W. J. H., & Zitman, F. (2010). Overweight, obesity, and depression. Archives of General Psychiatry, 67(3), 220–229.
Maddock, R. J., Garrett, A. S., & Buonocore, M. H. (2003). Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task. Human Brain Mapping, 18(1), 30–41. https://doi.org/10.1002/hbm.10075.
Malik, V. S., Willett, W. C., & Hu, F. B. (2013). Global obesity: Trends, risk factors and policy implications. Nature Reviews Endocrinology, 9(1), 13–27. https://doi.org/10.1038/nrendo.2012.199.
March, J. S., Parker, J. D. A., Sullivan, K., Stallings, P., & Conners, C. K. (1997). The multidimensional anxiety scale for children (MASC): Factor structure, reliability, and validity. Journal of the American Academy of Child and Adolescent Psychiatry, 36(4), 554–565. https://doi.org/10.1097/00004583-199704000-00019.
McLaughlin, T. (2012). Metabolic heterogeneity of obesity: Role of adipose tissue. International Journal of Obesity Supplements, 2(S1), S8–S10. https://doi.org/10.1038/ijosup.2012.3.
Mond, J. M., Hay, P. J., Rodgers, B., Owen, C., & Beumont, P. J. V. (2004). Validity of the eating disorder examination questionnaire (EDE-Q) in screening for eating disorders in community samples. Behaviour Research and Therapy, 42(5), 551–567. https://doi.org/10.1016/S0005-7967(03)00161-X.
Mumford, J. a., Horvath, S., Oldham, M. C., Langfelder, P., Geschwind, D. H., & Poldrack, R. a. (2010). Detecting network modules in fMRI time series: a weighted network analysis approach. NeuroImage, 52(4), 1465–1476. https://doi.org/10.1016/j.neuroimage.2010.05.047.
Nooner, K. B., Colcombe, S. J., Tobe, R. H., Mennes, M., Benedict, M. M., Moreno, A. L., Panek, L. J., Brown, S., Zavitz, S. T., Li, Q., Sikka, S., Gutman, D., Bangaru, S., Schlachter, R. T., Kamiel, S. M., Anwar, A. R., Hinz, C. M., Kaplan, M. S., Rachlin, A. B., Adelsberg, S., Cheung, B., Khanuja, R., Yan, C., Craddock, C. C., Calhoun, V., Courtney, W., King, M., Wood, D., Cox, C. L., Kelly, A. M. C., di Martino, A., Petkova, E., Reiss, P. T., Duan, N., Thomsen, D., Biswal, B., Coffey, B., Hoptman, M. J., Javitt, D. C., Pomara, N., Sidtis, J. J., Koplewicz, H. S., Castellanos, F. X., Leventhal, B. L., & Milham, M. P. (2012). The NKI-Rockland sample: A model for accelerating the pace of discovery science in psychiatry. Frontiers in Neuroscience, 6, 152. https://doi.org/10.3389/fnins.2012.00152.
Oren, A., Vos, L. E., Uiterwaal, C. S. P. M., Gorissen, W. H. M., Grobbee, D. E., & Bots, M. L. (2003). Change in body mass index from adolescence to young adulthood and increased carotid intima-media thickness at 28 years of age: The atherosclerosis risk in young adults study. International Journal of Obesity, 27(11), 1383–1390. https://doi.org/10.1038/sj.ijo.0802404.
Park, B., Seo, J., & Park, H. (2016). Functional brain networks associated with eating behaviors in obesity. Scientific Reports, 6, 23891. https://doi.org/10.1038/srep23891.
Park, B., Moon, T., & Park, H. (2018). Dynamic functional connectivity analysis reveals improved association between brain networks and eating behaviors compared to static analysis. Behavioural Brain Research, 337, 114–121. https://doi.org/10.1016/j.bbr.2017.10.001.
Rapuano, K. M., Huckins, J. F., Sargent, J. D., Heatherton, T. F., & Kelley, W. M. (2016). Individual differences in reward and somatosensory-motor brain regions correlate with adiposity in adolescents. Cerebral Cortex, 26(6), 2602–2611. https://doi.org/10.1093/cercor/bhv097.
Reinert, K. R. S., Po, E. K., & Barkin, S. L. (2013). The relationship between executive function and obesity in children and adolescents : A systematic literature review. Journal of Obesity, 2013(2), 1–10. https://doi.org/10.1159/000350031.
Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. NeuroImage, 52(3), 1059–1069. https://doi.org/10.1016/j.neuroimage.2009.10.003.
Salimi-Khorshidi, G., Douaud, G., Beckmann, C. F., Glasser, M. F., Griffanti, L., & Smith, S. M. (2014). Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers. NeuroImage, 90, 449–468. https://doi.org/10.1016/j.neuroimage.2013.11.046.
Santel, S., Baving, L., Krauel, K., Münte, T. F., & Rotte, M. (2006). Hunger and satiety in anorexia nervosa: fMRI during cognitive processing of food pictures. Brain Research, 1114(1), 138–148. https://doi.org/10.1016/j.brainres.2006.07.045.
Schwarz, A. J., & McGonigle, J. (2011). Negative edges and soft thresholding in complex network analysis of resting state functional connectivity data. NeuroImage, 55(3), 1132–1146. https://doi.org/10.1016/j.neuroimage.2010.12.047.
Ségonne, F., Pacheco, J., & Fischl, B. (2007). Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Transactions on Medical Imaging, 26(4), 518–529. https://doi.org/10.1109/TMI.2006.887364.
Shaw, M. E., Sachdev, P. S., Abhayaratna, W., Anstey, K. J., & Cherbuin, N. (2017). Body mass index is associated with cortical thinning with different patterns in mid- and late-life. International Journal of Obesity, 42, 455–461. https://doi.org/10.1038/ijo.2017.254.
Shott, M. E., Cornier, M.-A., Mittal, V. A., Pryor, T. L., Orr, J. M., Brown, M. S., & Frank, G. K. W. (2015). Orbitofrontal cortex volume and brain reward response in obesity. International Journal of Obesity, 39(2), 214–221. https://doi.org/10.1038/ijo.2014.121.
Siep, N., Roefs, A., Roebroeck, A., Havermans, R., Bonte, M., & Jansen, A. (2012). Fighting food temptations: The modulating effects of short-term cognitive reappraisal, suppression and up-regulation on mesocorticolimbic activity related to appetitive motivation. NeuroImage, 60(1), 213–220. https://doi.org/10.1016/j.neuroimage.2011.12.067.
Smith, S. M., Fox, P. T., Miller, K. L., Glahn, D. C., Fox, P. M., Mackay, C. E., Filippini, N., Watkins, K. E., Toro, R., Laird, A. R., & Beckmann, C. F. (2009). Correspondence of the brain’s functional architecture during activation and rest. Proceedings of the National Academy of Sciences of the United States of America, 106(31), 13040–13045. https://doi.org/10.1073/pnas.0905267106.
Stice, E., Spoor, S., Bohon, C., Veldhuizen, M., & Small, D. (2008). Relation of reward from food intake and anticipated food intake to obesity: A functional magnetic resonance imaging study. Journal of Abnormal Psychology, 117(4), 924–935. https://doi.org/10.1037/a0013600.Relation.
Stice, E., Yokum, S., Burger, K. S., Epstein, L. H., & Small, D. M. (2011). Youth at risk for obesity show greater activation of striatal and somatosensory regions to food. Journal of Neuroscience, 31(12), 4360–4366. https://doi.org/10.1523/JNEUROSCI.6604-10.2011.
Sysko, R., Walsh, B. T., Schebendach, J., & Wilson, G. T. (2005). Eating behavior among women with anorexia nervosa. American Journal of Clinical Nutrition, 82(2), 296–301.
Tataranni, P. A., & DelParigi, A. (2003). Functional neuroimaging: a new generation of human brain studies in obesity research. Obesity Reviews, 4(4), 229–238. https://doi.org/10.1046/j.1467-789X.2003.00111.x.
Tataranni, P. A., Gautier, J.-F., Chen, K., Uecker, A., Bandy, D., Salbe, A. D., et al. (1999). Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proceedings of the National Academy of Sciences of the United States of America, 96, 4569–4574. https://doi.org/10.1073/pnas.96.8.4569.
Tirosh, A., Shai, I., Afek, A., Dubnov-Raz, G., Ayalon, N., Gordon, B., Derazne, E., Tzur, D., Shamis, A., Vinker, S., & Rudich, A. (2011). Adolescent BMI trajectory and risk of diabetes versus coronary disease. The new england journal o f medicine original, 364(14), 1315–1325. https://doi.org/10.1056/NEJMoa1006992.
Tregellas, J. R., Wylie, K. P., Rojas, D. C., Tanabe, J., Martin, J., Kronberg, E., Cordes, D., & Cornier, M. A. (2011). Altered default network activity in obesity. Obesity, 19(12), 2316–2321. https://doi.org/10.1038/oby.2011.119.
Val-Laillet, D., Aarts, E., Weber, B., Ferrari, M., Quaresima, V., Stoeckel, L. E., Alonso-Alonso, M., Audette, M., Malbert, C. H., & Stice, E. (2015). Neuroimaging and neuromodulation approaches to study eating behavior and prevent and treat eating disorders and obesity. NeuroImage: Clinical, 8, 1–31. https://doi.org/10.1016/j.nicl.2015.03.016.
Walsh, B. T. (2011). The importance of eating behavior in eating disorders. Physiology and Behavior, 104(4), 525–529. https://doi.org/10.1016/j.physbeh.2011.05.007.
Wang, G.-J., Volkow, N. D., Felder, C., Fowler, J. S., Levy, A. V., Pappas, N. R., Wong, C. T., Zhu, W., & Netusil, N. (2002). Enhanced resting activity of the oral somatosensory cortex in obese subjects. Neuroreport, 13(9), 1151–1155. https://doi.org/10.1097/00001756-200207020-00016.
Whitaker, R. C., Wright, J. A., Pepe, M. S., Seidel, K. D., & Dietz, W. H. (1997). Predicting obesity in young adulthood from childhood. The New England Journal of Medicine, 337(13), 869–873. https://doi.org/10.1056/NEJM199709253371301.
Yoshimura, H., Kato, N., Sugai, T., Honjo, M., Sato, J., Segami, N., & Onoda, N. (2004). To-and-fro optical voltage signal propagation between the insular gustatory and parietal oral somatosensory areas in rat cortex slices. Brain Research, 1015(1–2), 114–121. https://doi.org/10.1016/j.brainres.2004.04.056.
Acknowledgements
This work was supported by the Institute for Basic Science (grant number IBS-R015-D1), the NRF (National Research Foundation of Korea, grant numbers NRF-2016H1A2A1907833, NRF-2016R1A2B4008545, NRF-2017R1A2B2009086, and NRF-2017R1A2B4007254), and the MIST (Ministry of Science and ICT), Korea, under the ITRC (Information Technology Research Center) support program (IITP-2019-2018-0-01798) supervised by the IITP (Institute for Information & communications Technology Promotion).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
All authors declare no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional review board and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 5.85 mb)
Rights and permissions
About this article
Cite this article
Park, By., Chung, CS., Lee, M.J. et al. Accurate neuroimaging biomarkers to predict body mass index in adolescents: a longitudinal study. Brain Imaging and Behavior 14, 1682–1695 (2020). https://doi.org/10.1007/s11682-019-00101-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-019-00101-y