Adiposity is associated with structural properties of the adolescent brain

NeuroImage

Volumn 103, Issue , 2014, Pages 192-201

  Schwartz, Deborah H ^a,b   Dickie, Erin ^a   Pangelinan, Melissa M ^a   Leonard, Gabriel ^c   Perron, Michel ^d   Pike, G Bruce ^e   Richer, Louis ^d   Veillette, Suzanne ^d,f   Pausova, Zdenka ^g   Paus, Tomáš ^a,b  

^a ROTMAN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITÉ DU QUÉBEC À CHICOUTIMI   (Canada)

^e UNIVERSITY OF CALGARY   (Canada)

^f Groupe ICOBES Recherche et Transfert   (Canada)

^g HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Fat mass; Intra abdominal fat; MRI signal contrast; MRI signal intensity; MTR; Obesity; Total body fat; Visceral fat

Indexed keywords

ADOLESCENT; AGE; ARTICLE; BODY FAT; BODY HEIGHT; CHILD; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIFFUSION WEIGHTED IMAGING; FEMALE; GRAY MATTER; HUMAN; INTRAABDOMINAL FAT; LIPID COMPOSITION; MALE; NEUROANATOMY; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OBESITY; PUBERTY; RADIOLOGICAL PARAMETERS; SEX DIFFERENCE; WHITE MATTER;

EID: 84907607966     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.09.030     Document Type: Article

References (95)

1. Abbott S.K., Else P.L., Atkins T.A., Hulbert A.J. Fatty acid composition of membrane bilayers: importance of diet polyunsaturated fat balance. Biochim. Biophys. Acta 2012, 1818:1309-1317. 10.1016/j.bbamem.2012.01.011.
2. Ancelin M.L., Ripoche E., Dupuy A.M., Samieri C., Rouaud O., Berr C., Carriere I., Ritchie K. Gender-specific associations between lipids and cognitive decline in the elderly. Eur. Neuropsychopharmacol. 2014, 24:1056-1066. (epub ahead). 10.1016/j.euroneuro.2014.02.003.
3. Aronne L.J. Epidemiology, morbidity, and treatment of overweight and obesity. J. Clin. Psychiatry 2001, 62(Suppl. 2):13-22.
4. Avants B.B., Epstein C.L., Grossman M., Gee J.C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 2008, 12:26-41. 10.1016/j.media.2007.06.004.
5. Beydoun M.A., Beydoun H.A., Wang Y. Obesity and central obesity as risk factors for incident dementia and its subtypes: a systematic review and meta-analysis. Obes. Rev. 2008, 9:204-218. 10.1111/j.1467-789X.2008.00473.x.
6. Bjermo H., Iggman D., Kullberg J., Dahlman I., Johansson L., Persson L., Berglund J., Pulkki K., Basu S., Uusitupa M., Rudling M., Arner P., Cederholm T., Ahlstrom H., Riserus U. Effects of n-6 PUFAs compared with SFAs on liver fat, lipoproteins, and inflammation in abdominal obesity: a randomized controlled trial. Am. J. Clin. Nutr. 2012, 95:1003-1012.
7. Blackmon K., Halgren E., Barr W.B., Carlson C., Devinsky O., DuBois J., Quinn B.T., French J., Kuzniecky R., Thesen T. Individual differences in verbal abilities associated with regional blurring of the left gray and white matter boundary. J. Neurosci. 2011, 31:15257-15263. 10.1523/JNEUROSCI.3039-11.2011.
8. Borg M.L., Omran S.F., Weir J., Meikle P.J., Watt M.J. Consumption of a high-fat diet, but not regular endurance exercise training, regulates hypothalamic lipid accumulation in mice. J. Physiol. 2012, 590:4377-4389. 10.1113/jphysiol.2012.233288.
9. Bradbury J. Docosahexaenoic acid (DHA): an ancient nutrient for the modern human brain. Nutrients 2011, 3:529-554. 10.3390/nu3050529.
10. Breger R.K., Yetkin F.Z., Fischer M.E., Papke R.A., Haughton V.M., Rimm A.A. T1 and T2 in the cerebrum: correlation with age, gender, and demographic factors. Radiology 1991, 181:545-547.
11. 14N quadrupolar relaxation. J. Chem. Phys. 1982, 77:1576-1599.
12. Camhi S.M., Katzmarzyk P.T. Differences in body composition between metabolically healthy obese and metabolically abnormal obese adults. Int. J. Obes. 2013, 38:1142-1145. 10.1038/ijo.2013.208.
13. Canadian Health Measures Survey Body Mass Index of Canadian Children and Youth, 2009 to 2011 2013, Statistics Canada, Ottawa.
14. Canadian Health Measures Survey Body Composition of Canadian Adults, 2009 to 2011 2013, Statistics Canada, Ottawa.
15. Carvalho M., Sampaio J.L., Palm W., Brankatschk M., Eaton S., Shevchenko A. Effects of diet and development on the Drosophila lipidome. Mol. Syst. Biol. 2012, 8:600. 10.1038/msb.2012.29.
16. Cazettes F., Tsui W.H., Johnson G., Steen R.G., Convit A. Systematic differences between lean and obese adolescents in brain spin-lattice relaxation time: a quantitative study. Am. J. Neuroradiol. 2011, 32:2037-2042. 10.3174/ajnr.A2698.
17. Ceckler T.L., Wolff S.D., Yip V., Simon S.A., Balaban R.S. Dynamic and chemical factors affecting water proton relaxation by macromolecules. J. Magn. Reson. 1992, 98:637-645. 10.1016/0022-2364(92)90018-3.
18. Chalon S. Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins Leukot. Essent. Fat. Acids 2006, 75:259-269. 10.1016/j.plefa.2006.07.005.
19. Collins D.L., Holmes C.J., Peters T.M., Evans A.C. Automatic 3-D model-based neuroanatomical segmentation. Hum. Brain Mapp. 1995, 3:190-208. 10.1002/hbm.460030304.
20. Couet C., Delarue J., Ritz P., Antoine J.M., Lamisse F. Effect of dietary fish oil on body fat mass and basal fat oxidation in healthy adults. Int. J. Obes. Relat. Metab. Disord. 1997, 21:637-643.
21. Dale A.M., Fischl B., Sereno M.I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999, 9:179-194. 10.1006/nimg.1998.0395.
22. Davies G.R., Ramani A., Dalton C.M., Tozer D.J., Wheeler-Kingshott C.A., Barker G.J., Thompson A.J., Miller D.H., Tofts P.S. Preliminary magnetic resonance study of the macromolecular proton fraction in white matter: a potential marker of myelin?. Mult. Scler. 2003, 9:246-249.
23. De Wilde M.C., Hogyes E., Kiliaan A.J., Farkas T., Luiten P.G., Farkas E. Dietary fatty acids alter blood pressure, behavior and brain membrane composition of hypertensive rats. Brain Res. 2003, 988:9-19.
24. Debette S., Beiser A., Hoffmann U., Decarli C., O'Donnell C.J., Massaro J.M., Au R., Himali J.J., Wolf P.A., Fox C.S., Seshadri S. Visceral fat is associated with lower brain volume in healthy middle-aged adults. Ann. Neurol. 2010, 68:136-144. 10.1002/ana.22062.
25. Dousset V., Grossman R.I., Ramer K.N., Schnall M.D., Young L.H., Gonzalez-Scarano F., Lavi E., Cohen J.A. Experimental allergic encephalomyelitis and multiple sclerosis: lesion characterization with magnetization transfer imaging. Radiology 1992, 182:483-491.
26. Driscoll I., Beydoun M.A., An Y., Davatzikos C., Ferrucci L., Zonderman A.B., Resnick S.M. Midlife obesity and trajectories of brain volume changes in older adults. Hum. Brain Mapp. 2012, 33:2204-2210. 10.1002/hbm.21353.
27. Fox C.S., Massaro J.M., Hoffmann U., Pou K.M., Maurovich-Horvat P., Liu C.Y., Vasan R.S., Murabito J.M., Meigs J.B., Cupples L.A., D'Agostino R.B., O'Donnell C.J. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation 2007, 116:39-48. 10.1161/CIRCULATIONAHA.106.675355.
28. Fujioka S., Matsuzawa Y., Tokunaga K., Tarui S. Contribution of intra-abdominal fat accumulation to the impairment of glucose and lipid metabolism in human obesity. Metabolism 1987, 36:54-59.
29. 2+-triggered membrane fusion. Integrating studies of proteins and lipids. Ann. N. Y. Acad. Sci. 2009, 1152:121-134. 10.1111/j.1749-6632.2008.03993.x.
30. Gollisch K.S., Brandauer J., Jessen N., Toyoda T., Nayer A., Hirshman M.F., Goodyear L.J. Effects of exercise training on subcutaneous and visceral adipose tissue in normal- and high-fat diet-fed rats. Am. J. Physiol. Endocrinol. Metab. 2009, 297:495-504. 10.1152/ajpendo.90424.2008.
31. Goodwin K., Syme C., Abrahamowicz M., Leonard G.T., Richer L., Perron M., Veillette S., Gaudet D., Paus T., Pausova Z. Routine clinical measures of adiposity as predictors of visceral fat in adolescence: a population-based magnetic resonance imaging study. PLoS One 2013, 8:e79896. 10.1371/journal.pone.0079896.
32. Grabner G., Janke A.L., Budge M.M., Smith D., Pruessner J., Collins D.L. Symmetric atlasing and model based segmentation: an application to the hippocampus in older adults. Med. Image Comput. Comput. Assist. Interv. 2006, 9:58-66.
33. Gunstad J., Paul R.H., Cohen R.A., Tate D.F., Spitznagel M.B., Grieve S., Gordon E. Relationship between body mass index and brain volume in healthy adults. Int. J. Neurosci. 2008, 118:1582-1593. 10.1080/00207450701392282.
34. Haltia L.T., Viljanen A., Parkkola R., Kemppainen N., Rinne J.O., Nuutila P., Kaasinen V. Brain white matter expansion in human obesity and the recovering effect of dieting. J. Clin. Endocrinol. Metab. 2007, 92:3278-3284. 10.1210/jc.2006-2495.
35. Harrison N.A., Doeller C.F., Voon V., Burgess N., Critchley H.D. Peripheral inflammation acutely impairs human spatial memory via actions on medial temporal lobe glucose metabolism. Biol. Psychiatry 2014, 10.1016/j.biopsych.2014.01.005.
36. Ho A.J., Stein J.L., Hua X., Lee S., Hibar D.P., Leow A.D., Dinov I.D., Toga A.W., Saykin A.J., Shen L., Foroud T., Pankratz N., Huentelman M.J., Craig D.W., Gerber J.D., Allen A.N., Corneveaux J.J., Stephan D.A., DeCarli C.S., DeChairo B.M., Potkin S.G., Jack C.R., Weiner M.W., Raji C.A., Lopez O.L., Becker J.T., Carmichael O.T., Thompson P.M., The Alzhiemer's Disease Neuroimaging Initiative A commonly carried allele of the obesity-related FTO gene is associated with reduced brain volume in the healthy elderly. Proc. Natl. Acad. Sci. 2010, 107:8404-8409. 10.1073/pnas.0910878107.
37. Horstmann A., Busse F., Mathar D., Mueller K., Lepsien J., Schloegl H., Kabisch S., Kratzsch J., Neumann J., Stumvoll M., Villringer A., Pleger B. Obesity-related differences between women and men in brain structure and goal-directed behavior. Front. Hum. Neurosci. 2011, 5. 10.3389/fnhum.2011.00058.
38. Isaac V., Sim S., Zheng H., Zagorodnov V., Tai S.E., Chee M. Adverse associations between visceral adiposity, brain structure, and cognitive performance in healthy elderly. Front. Aging Neurosci. 2011, 3:1-8. 10.3389/fnagi.2011.00012.
39. Janssen C.I., Kiliaan A.J. Long-chain polyunsaturated fatty acids (LCPUFA) from genesis to senescence: the influence of LCPUFA on neural development, aging, and neurodegeneration. Prog. Lipid Res. 2014, 53:1-17. 10.1016/j.plipres.2013.10.002.
40. Kabir M., Skurnik G., Naour N., Pechtner V., Meugnier E., Rome S., Quignard-Boulange A., Vidal H., Slama G., Clement K., Guerre-Millo M., Rizkalla S.W. Treatment for 2 mo with n 3 polyunsaturated fatty acids reduces adiposity and some atherogenic factors but does not improve insulin sensitivity in women with type 2 diabetes: a randomized controlled study. Am. J. Clin. Nutr. 2007, 86:1670-1679.
41. Kamijo K., Khan N.A., Pontifex M.B., Scudder M.R., Drollette E.S., Raine L.B., Evans E.M., Castelli D.M., Hillman C.H. The relation of adiposity to cognitive control and scholastic achievement in preadolescent children. Obesity 2012, 10.1038/oby.2012.112.
42. Karmi A., Iozzo P., Viljanen A., Hirvonen J., Fielding B.A., Virtanen K., Oikonen V., Kemppainen J., Viljanen T., Guiducci L., Haaparanta-Solin M., Nagren K., Solin O., Nuutila P. Increased brain fatty acid uptake in metabolic syndrome. Diabetes 2010, 59:2171-2177. 10.2337/db09-0138.
43. Kim J.Y., Park J.Y., Kim O.Y., Ham B.M., Kim H.-J., Kwon D.Y., Jang Y., Lee J.H. Metabolic profiling of plasma in overweight/obese and lean men using ultra performance liquid chromatography and Q-TOF mass spectrometry (UPLC-Q-TOF MS). J. Proteome Res. 2010, 9:4368-4375. 10.1021/pr100101p.
44. Kucharczyk W., Macdonald P.M., Stanisz G.J., Henkelman R.M. Relaxivity and magnetization transfer of white matter lipids at MR imaging: importance of cerebrosides and pH. Radiology 1994, 192:521-529. 10.1148/radiology.192.2.8029426.
45. Ledesma M.D., Martin M.G., Dotti C.G. Lipid changes in the aged brain: effect on synaptic function and neuronal survival. Prog. Lipid Res. 2012, 51:23-35. 10.1016/j.plipres.2011.11.004.
46. Levant B., Ozias M.K., Guilford B.L., Wright D.E. Streptozotocin-induced diabetes partially attenuates the effects of a high-fat diet on liver and brain fatty acid composition in mice. Lipids 2013, 48:939-948. 10.1007/s11745-013-3817-z.
47. Loef M., Walach H. Midlife obesity and dementia: meta-analysis and adjusted forecast of dementia prevalence in the United States and China. Obesity 2013, 21:E51-E55. 10.1002/oby.20037.
48. McRobbie D.W. MRI From Picture to Proton 2007, Cambridge University Press, New York. 2nd ed.
49. Mottershead J.P., Schmierer K., Clemence M., Thornton J.S., Scaravilli F., Barker G.J., Tofts P.S., Newcombe J., Cuzner M.L., Ordidge R.J., McDonald W.I., Miller D.H. High field MRI correlates of myelin content and axonal density in multiple sclerosis-a post-mortem study of the spinal cord. J. Neurol. 2003, 250:1293-1301. 10.1007/s00415-003-0192-3.
50. Mueller K., Anwander A., Moller H.E., Horstmann A., Lepsien J., Busse F., Mohammadi S., Schroeter M.L., Stumvoll M., Villringer A., Pleger B. Sex-dependent influences of obesity on cerebral white matter investigated by diffusion-tensor imaging. PLoS One 2011, 6:e18544. 10.1371/journal.pone.0018544.
51. Muller M.J., Lagerpusch M., Enderle J., Schautz B., Heller M., Bosy-Westphal A. Beyond the body mass index: tracking body composition in the pathogenesis of obesity and the metabolic syndrome. Obes. Rev. 2012, 13(Suppl. 2):6-13. 10.1111/j.1467-789X.2012.01033.x.
52. Murase T., Mizuno T., Omachi T., Onizawa K., Komine Y., Kondo H., Hase T., Tokimitsu I. Dietary diacylglycerol suppresses high fat and high sucrose diet-induced body fat accumulation in C57BL/6J mice. J. Lipid Res. 2001, 42:372-378.
53. Ogden C.L., Carroll M.D., Kit B.K., Flegal K.M. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 2014, 311:806-814. 10.1001/jama.2014.732.
54. Pausova Z., Mahboubi A., Abrahamowicz M., Leonard G.T., Perron M., Richer L., Veillette S., Gaudet D., Paus T. Sex differences in the contributions of visceral and total body fat to blood pressure in adolescence. Hypertension 2012, 59:572-579. 10.1161/HYPERTENSIONAHA.111.180372.
55. Pausova Z., Paus T., Abrahamowicz M., Almerigi J., Arbour N., Bernard M., Gaudet D., Hanzalek P., Hamet P., Evans A.C., Kramer M., Laberge L., Leal S.M., Leonard G., Lerner J., Lerner R.M., Mathieu J., Perron M., Pike B., Pitiot A., Richer L., Séguin J.R., Syme C., Toro R., Tremblay R.E., Veillette S., Watkins K. Genes, maternal smoking, and the offspring brain and body during adolescence: design of the Saguenay Youth Study. Hum. Brain Mapp. Spec. Issue Genomic Imaging 2007, 28:502-518. 10.1002/hbm.20402.
56. Perrin J.S., Hervé P.-Y., Leonard G., Perron M., Pike G.B., Pitiot A., Richer L., Veillette S., Pausova Z., Paus T. Growth of white matter in the adolescent brain: role of testosterone and androgen receptor. J. Neurosci. 2008, 28:9519-9524. 10.1523/JNEUROSCI.1212-08.2008.
57. Perrin J.S., Leonard G., Perron M., Pike G.B., Pitiot A., Richer L., Veillette S., Pausova Z., Paus T. Sex differences in the growth of white matter during adolescence. Neuroimage 2009, 45:1055-1066. 10.1016/j.neuroimage.2009.01.023.
58. Peterson A., Crockett L., Richards M., Boxer A. A self-report measure of pubertal status. J. Youth Adolesc. 1988, 17:117-133.
59. Petursdottir A.L., Farr S.A., Morley J.E., Banks W.A., Skuladottir G.V. Effect of dietary n-3 polyunsaturated fatty acids on brain lipid fatty acid composition, learning ability, and memory of senescence-accelerated mouse. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2008, 63:1153-1160.
60. Pike G.B. Pulsed magnetization transfer contrast in gradient echo imaging: a two-pool analytic description of signal response. Magn. Reson. Med. 1996, 36:95-103.
61. Piomelli D., Astarita G., Rapaka R. A neuroscientist's guide to lipidomics. Nat. Rev. Neurosci. 2007, 8:743-754. 10.1038/nrn2233.
62. Podo F., Blasie J.K. Proton magnetic relaxation studies of mixed phosphatidylcholine/fatty acid and mixed phosphatidylcholine bimolecular bilayers. Biochim. Biophys. Acta 1976, 419:1-18.
63. Pou K.M., Massaro J.M., Hoffmann U., Vasan R.S., Maurovich-Horvat P., Larson M.G., Keaney J.F., Meigs J.B., Lipinska I., Kathiresan S., Murabito J.M., O'Donnell C.J., Benjamin E.J., Fox C.S. Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham Heart Study. Circulation 2007, 116:1234-1241. 10.1161/CIRCULATIONAHA.107.710509.
64. Raji C.A., Ho A.J., Parikshak N.N., Becker J.T., Lopez O.L., Kuller L.H., Hua X., Leow A.D., Toga A.W., Thompson P.M. Brain structure and obesity. Hum. Brain Mapp. 2010, 31:353-364. 10.1002/hbm.20870.
65. Rasgon N.L., Kenna H.A., Wroolie T.E., Kelley R., Silverman D., Brooks J., Williams K.E., Powers B.N., Hallmayer J., Reiss A. Insulin resistance and hippocampal volume in women at risk for Alzheimer's disease. Neurobiol. Aging 2011, 32:1942-1948. 10.1016/j.neurobiolaging.2009.12.005.
66. Ruzickova J., Rossmeisl M., Prazak T., Flachs P., Sponarova J., Vecka M., Tvrzicka E., Bryhn M., Kopecky J. Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids 2004, 39:1177-1185.
67. Salat D.H., Chen J.J., van der Kouwe A.J., Greve D.N., Fischl B., Rosas H.D. Hippocampal degeneration is associated with temporal and limbic gray matter/white matter tissue contrast in Alzheimer's disease. Neuroimage 2011, 54:1795-1802. 10.1016/j.neuroimage.2010.10.034.
68. Salat D.H., Lee S.Y., van der Kouwe A.J., Greve D.N., Fischl B., Rosas H.D. Age-associated alterations in cortical gray and white matter signal intensity and gray to white matter contrast. Neuroimage 2009, 48:21-28. 10.1016/j.neuroimage.2009.06.074.
69. Schwartz D.H., Leonard G., Perron M., Richer L., Syme C., Veillette S., Pausova Z., Paus T. Visceral fat is associated with lower executive functioning in adolescents. Int. J. Obes. 2013, 37:1336-1343.
70. Sena A., Sarlieve L.L., Rebel G. Brain myelin of genetically obese mice. J. Neurol. Sci. 1985, 68:233-243.
71. Shaw P., Kabani N.J., Lerch J.P., Eckstrand K., Lenroot R., Gogtay N., Greenstein D., Clasen L., Evans A., Rapoport J.L., Giedd J.N., Wise S.P. Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci. 2008, 28:3586-3594. 10.1523/JNEUROSCI.5309-07.2008.
72. Shirtcliff E.A., Dahl R.E., Pollak S.D. Pubertal development: correspondence between hormonal and physical development. Child Dev. 2009, 80:327-337. 10.1111/j.1467-8624.2009.01263.x.
73. Sled J.G., Zijdenbos A.P., Evans A.C. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging 1998, 17:87-97. 10.1109/42.668698.
74. Sowell E.R., Thompson P.M., Leonard C.M., Welcome S.E., Kan E., Toga A.W. Longitudinal mapping of cortical thickness and brain growth in normal children. J. Neurosci. 2004, 24:8223-8231. 10.1523/JNEUROSCI.1798-04.2004.
75. Stanek K.M., Grieve S.M., Brickman A.M., Korgaonkar M.S., Paul R.H., Cohen R.A., Gunstad J.J. Obesity is associated with reduced white matter integrity in otherwise healthy adults. Obesity 2011, 19:500-504. 10.1038/oby.2010.312.
76. Stanisz G.J., Webb S., Munro C.A., Pun T., Midha R. MR properties of excised neural tissue following experimentally induced inflammation. Magn. Reson. Med. 2004, 51:473-479. 10.1002/mrm.20008.
77. Steen R.G., Gronemeyer S.A., Taylor J.S. Age-related changes in proton T1 values of normal human brain. J. Magn. Reson. Imaging 1995, 5:43-48. 10.1002/jmri.1880050111.
78. Stuber C., Morawski M., Schafer A., Labadie C., Wahnert M., Leuze C., Streicher M., Barapatre N., Reimann K., Geyer S., Spemann D., Turner R. Myelin and iron concentration in the human brain: a quantitative study of MRI contrast. Neuroimage 2014, 93(Pt. 1):95-106. 10.1016/j.neuroimage.2014.02.026.
79. Syme C., Abrahamowicz M., Leonard G.T., Perron M., Pitiot A., Qiu X., Richer L., Totman J., Veillette S., Xiao Y., Gaudet D., Paus T., Pausova Z. Intra-abdominal adiposity and individual components of the metabolic syndrome in adolescence: sex differences and underlying mechanisms. Arch. Pediatr. Adolesc. Med. 2008, 162:453-461.
80. Taki Y., Thyreau B., Kinomura S., Sato K., Goto R., Wu K., Kakizaki M., Tsuji I., Kawashima R., Fukuda H. Correlation between high-sensitivity C-reactive protein and brain gray matter volume in healthy elderly subjects. Hum. Brain Mapp. 2013, 34:2418-2424. 10.1002/hbm.22073.
81. Tamnes C.K., Ostby Y., Fjell A.M., Westlye L.T., Due-Tonnessen P., Walhovd K.B. Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb. Cortex 2010, 20:534-548. 10.1093/cercor/bhp118.
82. Tchernof A., Despres J.P. Pathophysiology of human visceral obesity: an update. Physiol. Rev. 2013, 93:359-404. 10.1152/physrev.00033.2011.
83. Thambisetty M., Beason-Held L.L., An Y., Kraut M., Metter J., Egan J., Ferrucci L., O'Brien R., Resnick S.M. Impaired glucose tolerance in midlife and longitudinal changes in brain function during aging. Neurobiol. Aging 2013, 34:2271-2276. 10.1016/j.neurobiolaging.2013.03.025.
84. Tohka J., Zijdenbos A., Evans A. Fast and robust parameter estimation for statistical partial volume models in brain MRI. Neuroimage 2004, 23:84-97. 10.1016/j.neuroimage.2004.05.007.
85. Verstynen T.D., Weinstein A.M., Schneider W.W., Jakicic J.M., Rofey D.L., Erickson K.I. Increased body mass index is associated with a global and distributed decrease in white matter microstructural integrity. Psychosom. Med. 2012, 74:682-690. 10.1097/PSY.0b013e318261909c.
86. Walther K., Birdsill A.C., Glisky E.L., Ryan L. Structural brain differences and cognitive functioning related to body mass index in older females. Hum. Brain Mapp. 2010, 31:1052-1064. 10.1002/hbm.20916.
87. Ward M.A., Bendlin B.B., McLaren D.G., Hess T.M., Gallagher C.L., Kastman E.K., Rowley H.A., Asthana S., Carlsson C.M., Sager M.A., Johnson S.C. Low HDL cholesterol is associated with lower gray matter volume in cognitively healthy adults. Front. Aging Neurosci. 2010, 2. 10.3389/fnagi.2010.00029.
88. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112:1796-1808. 10.1172/JCI19246.
89. Weise C.M., Thiyyagura P., Reiman E.M., 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, 64:712-721. 10.1016/j.neuroimage.2012.09.005.
90. Westlye L.T., Walhovd K.B., Dale A.M., Bjornerud A., Due-Tonnessen P., Engvig A., Grydeland H., Tamnes C.K., Ostby Y., Fjell A.M. Differentiating maturational and aging-related changes of the cerebral cortex by use of thickness and signal intensity. Neuroimage 2010, 52:172-185. 10.1016/j.neuroimage.2010.03.056.
91. Westlye L.T., Walhovd K.B., Dale A.M., Espeseth T., Reinvang I., Raz N., Agartz I., Greve D.N., Fischl B., Fjell A.M. Increased sensitivity to effects of normal aging and Alzheimer's disease on cortical thickness by adjustment for local variability in gray/white contrast: a multi-sample MRI study. Neuroimage 2009, 47:1545-1557. 10.1016/j.neuroimage.2009.05.084.
92. Whitmer R.A., Gunderson E.P., Barrett-Connor E., Quesenberry C.P., Yaffe K. Obesity in middle age and future risk of dementia: a 27year longitudinal population based study. BMJ 2005, 330:1360. 10.1136/bmj.38446.466238.E0.
93. Yamashita K., Kondo T., Osugi S., Shimokata K., Maeda K., Okumura N., Matsudaira K., Shintani S., Muramatsu T., Matsushita K., Murohara T. The significance of measuring body fat percentage determined by bioelectrical impedance analysis for detecting subjects with cardiovascular disease risk factors. Circ. J. 2012, 76:2435-2442.
94. Yokum S., Ng J., Stice E. Relation of regional gray and white matter volumes to current BMI and future increases in BMI: a prospective MRI study. Int. J. Obes. 2012, 36:656-664. 10.1038/ijo.2011.175.
95. Zijdenbos A.P., Forghani R., Evans A.C. Automatic "pipeline" analysis of 3-D MRI data for clinical trials: application to multiple sclerosis. IEEE Trans. Med. Imaging 2002, 21:1280-1291. 10.1109/TMI.2002.806283.