Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-23T10:37:11.777Z Has data issue: false hasContentIssue false

Increased body mass index makes an impact on brain white-matter integrity in adults with remitted first-episode mania

Published online by Cambridge University Press:  26 April 2013

C. N. Kuswanto
Affiliation:
Research Department, Institute of Mental Health, Singapore
M. Y. Sum
Affiliation:
Research Department, Institute of Mental Health, Singapore
G. L. Yang
Affiliation:
Biomedical Imaging Laboratory, Singapore Bioimaging Consortium, Agency for Science, Technology and Research, Singapore
W. L. Nowinski
Affiliation:
Biomedical Imaging Laboratory, Singapore Bioimaging Consortium, Agency for Science, Technology and Research, Singapore
R. S. McIntyre
Affiliation:
Mood Disorders Psychopharmacology Unit, University Health Network, University of Toronto, Toronto, ON, Canada
K. Sim*
Affiliation:
Research Department, Institute of Mental Health, Singapore Yong Loo Lin School of Medicine, National University of Singapore, Singapore
*
*Address for correspondence: K. Sim, Department of General Psychiatry, Institute of Mental Health/Woodbridge Hospital, 10, Buangkok View, Singapore539747. (Email: kang_sim@imh.com.sg)

Abstract

Background

Obesity is increasingly prevalent in bipolar disorder (BD) but data about the impact of elevated body mass index (BMI) on brain white-matter integrity in BD are sparse. Based on extant literature largely from structural magnetic resonance imaging (MRI) studies, we hypothesize that increased BMI is associated with decreased fractional anisotropy (FA) in the frontal, temporal, parietal and occipital brain regions early in the course of BD.

Method

A total of 26 euthymic adults (12 normal weight and 14 overweight/obese) with remitted first-episode mania (FEM) and 28 controls (13 normal weight and 15 overweight/obese) matched for age, handedness and years of education underwent structural MRI and diffusion tensor imaging scans.

Results

There are significant effects of diagnosis by BMI interactions observed especially in the right parietal lobe (adjusted F1,48 = 5.02, p = 0.030), occipital lobe (adjusted F1,48 = 10.30, p = 0.002) and temporal lobe (adjusted F1,48 = 7.92, p = 0.007). Specifically, decreased FA is found in the right parietal (F1,23 = 5.864, p = 0.023) and occipital lobes (F1,23 = 4.397, p = 0.047) within overweight/obese patients compared with normal-weight patients with FEM. Compared with overweight/obese controls, decreased FA is observed in right parietal (F1,25 = 6.708, p = 0.015), temporal (F1,25 = 10.751, p = 0.003) and occipital (F1,25 = 9.531, p = 0.005) regions in overweight/obese patients with FEM.

Conclusions

Our findings suggest that increased BMI affects temporo-parietal-occipital brain white-matter integrity in FEM. This highlights the need to further elucidate the relationship between obesity and other neural substrates (including subcortical changes) in BD which may clarify brain circuits subserving the association between obesity and clinical outcomes in BD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Atmaca, M, Ozdemir, H, Cetinkaya, S, Parmaksiz, S, Belli, H, Poyraz, AK, Tezcan, E, Ogur, E (2007). Cingulate gyrus volumetry in drug free bipolar patients and patients treated with valproate or valproate and quetiapine. Journal of Psychiatric Research 41, 821827.Google Scholar
Bartzokis, G, Lu, PH, Amar, CP, Raven, EP, Detore, NR, Altshuler, LL, Mintz, J, Ventura, J, Casaus, LR, Luo, JS, Subotnik, KL, Nuechterlein, KH (2011). Long acting injection versus oral risperidone in first-episode schizophrenia: differential impact on white matter myelination trajectory. Schizophrenia Research 132, 3541.CrossRefGoogle ScholarPubMed
Bobb, JF, Schwartz, BS, Davatzikos, C, Caffo, B (2012). Cross-sectional and longitudinal association of body mass index and brain volume. Human Brain Mapping. Published online 24 09 2012 . doi:10.1002/hbm.22159.Google Scholar
Bond, DJ, Lang, DJ, Noronha, MM, Kunz, M, Torres, IJ, Su, W, Honer, WG, Lam, RW, Yatham, LN (2011). The association of elevated body mass index with reduced brain volumes in first-episode mania. Biological Psychiatry 70, 381387.Google Scholar
Chan, WY, Yang, GL, Chia, MY, Woon, PS, Lee, J, Keefe, R, Sitoh, YY, Nowinski, WL, Sim, K (2010). Cortical and subcortical white matter abnormalities in adults with remitted first-episode mania revealed by Tract-Based Spatial Statistics. Bipolar Disorders 12, 383389.Google Scholar
Enzinger, C, Fazekas, F, Matthews, PM, Ropele, S, Schmidt, H, Smith, S, Schmidt, R (2005). Risk factors for progression of brain atrophy in aging: six-year follow-up of normal subjects. Neurology 64, 17041711.CrossRefGoogle ScholarPubMed
Fagiolini, A, Kupfer, DJ, Houck, PR, Novick, DM, Frank, E (2003). Obesity as a correlate of outcome in patients with bipolar disorder. American Journal of Psychiatry 160, 112117.CrossRefGoogle Scholar
Fagiolini, A, Kupfer, DJ, Rucci, P, Scott, JA, Novick, DM, Frank, E (2004). Suicide attempts and ideation in patients with bipolar I disorder. Journal of Clinical Psychiatry 65, 509514.CrossRefGoogle ScholarPubMed
Farooqi, IS, Bullmore, E, Keogh, J, Gillard, J, O'Rahilly, S, Fletcher, PC (2007). Leptin regulates striatal regions and human eating behavior. Science 317, 1355.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1994). Structured Clinical Interview for DSM-IV Axis I Disorders-Patient Version (SCID-P). American Psychiatric Press: Washington, DC.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (2002). Structured Clinical Interview for DSM-IV Axis I Disorders-Non-Patient Version (SCID-I/NP). New York State Psychiatric Institute: New York.Google Scholar
Fischl, B, Salat, DH, 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, AM (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341355.Google Scholar
Gibson, CD, Carnell, S, Ochner, CN, Geliebter, A (2010). Neuroimaging, gut peptides and obesity: novel studies of the neurobiology of appetite. Journal of Neuroendocrinology 22, 833845.CrossRefGoogle ScholarPubMed
Goldstein, BI, Liu, SM, Zivkovic, N, Schaffer, A, Chien, LC, Blanco, C (2011). The burden of obesity among adults with bipolar disorder in the United States. Bipolar Disorders 13, 387395.Google Scholar
Gunstad, J, Paul, RH, Cohen, RA, Tate, DF, Gordon, E (2006). Obesity is associated with memory deficits in young and middle-aged adults. Eating and Weight Disorders 11, e15e19.Google Scholar
Gunstad, J, Paul, RH, Cohen, RA, Tate, DF, Spitznagel, MB, Gordon, E (2007). Elevated body mass index is associated with executive dysfunction in otherwise healthy adults. Comprehensive Psychiatry 48, 5761.CrossRefGoogle ScholarPubMed
Haltia, LT, Viljanen, A, Parkkola, R, Kemppainen, N, Rinne, JO, Nuutila, P, Kaasinen, V (2007). Brain white matter expansion in human obesity and the recovering effect of dieting. Journal of Clinical Endocrinology and Metabolism 92, 32783284.CrossRefGoogle ScholarPubMed
Heng, S, Song, AW, Sim, K (2010). White matter abnormalities in bipolar studies: insights from diffusion tensor imaging studies. Journal of Neural Transmission 117, 639654.Google Scholar
Ho, AJ, Stein, JL, Hua, X, Lee, S, Hibar, DP, Leow, AD, Dinov, ID, Toga, AW, Saykin, AJ, Shen, L, Foroud, T, Pankratz, N, Huentelman, MJ, Craig, DW, Gerber, JD, Allen, AN, Corneveaux, JJ, Stephan, DA, DeCarli, CS, DeChairo, BM, Potkin, SG, Jack, CR Jr, Weiner, MW, Raji, CA, Lopez, OL, Becker, JT, Carmichael, OT, Thompson, PM, Alzheimer's Disease Neuroimaging Initiative (2010). A commonly carried allele of the obesity-related FTO gene is associated with reduced brain volume in the healthy elderly. Proceedings of the National Academy of Sciences USA 107, 84048409.Google Scholar
Hoth, FK, Tate, DF, Poppas, A, Forman, DE, Gunstad, J, Moser, DJ, Paul, RH, Jefferson, AL, Haley, AP, Cohen, RA (2007). Endothelial function and white matter hyperintensities in older adults with cardiovascular disease. Stroke 38, 308312.Google Scholar
Jiang, H, van Zijl, PC, Kim, J, Pearlson, GD, Mori, S (2006). DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Computer Methods and Programs in Biomedicine 81, 106116.Google Scholar
Katsumata, T, Otori, T, Nishiyama, Y, Okubo, S, Nishiyama, Y, Nagayama, H, Ueda, M, Utsumi, K, Yamazaki, M, Komaba, Y, Katsura, K, Katayama, Y (2010). Correlation between insulin resistance and white matter lesions among non-diabetic patients with ischemic stroke. Neurological Research 32, 743747.CrossRefGoogle ScholarPubMed
Kempton, MJ, Geddes, JR, Ettinger, U, Williams, SC, Grasby, PM (2008). Meta-analysis, database, and meta-regression of 98 structural imaging studies in bipolar disorder. Archives of General Psychiatry 65, 10171032.Google Scholar
Kodl, CT, Franc, DT, Rao, JP, Anderson, FS, Thomas, W, Mueller, BA, Lim, KO, Seaquist, ER (2008). Diffusion tensor imaging identifies deficits in white matter microstructure in subjects with type 1 diabetes that correlate with reduced neurocognitive function. Diabetes 57, 30833089.Google Scholar
Magalhães, PV, Kapczinski, F, Nierenberg, AA, Deckersbach, T, Weisinger, D, Dodds, S, Berk, M (2012). Illness burden and medical comorbidity in the Systematic Treatment Enhancement Program for Bipolar Disorder. Acta Psychiatrica Scandinavia 125, 303308.Google Scholar
May, A (2011). Experience-dependent structural plasticity in the adult human brain. Trends in Cognitive Sciences 15, 475482.Google Scholar
McIntyre, RS, Kenna, HA, Nguyen, HT, Law, CW, Sultan, F, Woldeyohannes, HO, Adams, AK, Cheng, JS, Lourenco, M, Kennedy, SH, Rasgon, NL (2010). Brain volume abnormalities and neurocognitive deficits in diabetes mellitus: points of pathophysiological commonality with mood disorders? Advances in Therapy 27, 6380.Google Scholar
McIntyre, RS, Vagic, D, Swartz, SA, Soczynska, JK, Woldeyohannes, HO, Voruganti, LP, Konarski, JZ (2008). Insulin, insulin-like growth factors and incretins: neural homeostatic regulators and treatment opportunities. CNS Drugs 22, 443453.Google Scholar
Moore, GJ, Bebchuk, JM, Wilds, IB, Chen, G, Manji, HK (2000). Lithium-induced increase in human brain grey matter. Lancet 356, 12411242.CrossRefGoogle ScholarPubMed
Mueller, K, Anwander, A, Möller, HE, Horstmann, A, Lepsien, J, Busse, F, Mohammadi, S, Schroeter, ML, Stumvoll, M, Villringer, A, Pleger, B (2011). Sex-dependent influences of obesity on cerebral white matter investigated by diffusion-tensor imaging. PLoS One 11, e18544.CrossRefGoogle Scholar
Osby, U, Brandt, L, Correia, N, Correia, N, Ekbom, A, Sparén, P (2001). Excess mortality in bipolar and unipolar disorder in Sweden. Archives of General Psychiatry 58, 844850.Google Scholar
Pannacciulli, N, Del Parigi, A, Chen, K, Le, DS, Reiman, EM, Tataranni, PA (2006). Brain abnormalities in human obesity: a voxel-based morphometric study. Neuroimage 31, 14191425.Google Scholar
Rosenberg, GA (2009). Inflammation and white matter damage in vascular cognitive impairment. Stroke 40, S20S23.Google Scholar
Selemon, LD, Lidow, MS, Goldman-Rakic, PS (1999). Increased volume and glial density in primate prefrontal cortex associated with chronic antipsychotic drug exposure. Biological Psychiatry 46, 161172.Google Scholar
Soreca, I, Rosano, C, Jennings, JR, Sheu, LK, Kuller, LH, Matthews, KA, Aizenstein, HJ, Gianaros, PJ (2009). Gain in adiposity across 15 years is associated with reduced gray matter volume in healthy women. Psychosomatic Medicine 71, 485490.Google Scholar
Stanek, KM, Grieve, SM, Brickman, AM, Korgaonkar, MS, Paul, RH, Cohen, RA, Gunstad, JJ (2011). Obesity is associated with reduced white matter integrity in otherwise healthy adults. Obesity 19, 500504.Google Scholar
Taki, Y, Kinomura, S, Sato, K, Inoue, K, Goto, R, Okada, K, Uchida, S, Kawashima, R, Fukuda, H (2008). Relationship between body mass index and gray matter volume in 1,428 healthy individuals. Obesity 16, 119124.CrossRefGoogle Scholar
Tohen, M, Frank, E, Bowden, CL, Colom, F, Ghaemi, SN, Yatham, LN, Malhi, GS, Calabrese, JR, Nolen, WA, Vieta, E, Kapczinski, F, Goodwin, GM, Suppes, T, Sachs, GS, Chengappa, KR, Grunze, H, Mitchell, PB, Kanba, S, Berk, M (2009). The International Society for Bipolar Disorders (ISBD) Task Force report on the nomenclature of course and outcome in bipolar disorders. Bipolar Disorders 11, 453473.Google Scholar
Vederine, F, Wessa, M, Leboyer, M, Houenou, J (2011). A meta-analysis of whole-brain diffusion tensor imaging studies in bipolar disorder. Progress in Neuro-psychopharmacology and Biological Psychiatry 35, 18201826.CrossRefGoogle ScholarPubMed
Verstynen, TD, Weinstein, AM, Schneider, WW, Jakicic, JM, Rofey, DL, Erickson, KI (2012). Increased body mass index is associated with a global and distributed decrease in white matter microstructural integrity. Psychosomatic Medicine 74, 682690.Google Scholar
Vita, A, De Peri, L, Sacchetti, E (2009). Gray matter, white matter, brain, and intracranial volumes in first-episode bipolar disorder: a meta-analysis of magnetic resonance imaging studies. Bipolar Disorders 11, 807814.Google Scholar
WHO Expert Consultation (2004). Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363, 157163.Google Scholar
World Health Organization, International Association for the Study of Obesity, International Obesity Task Force (2000). The Asia-Pacific Perspective: Redefining Obesity and its Treatment. Health Communications Australia: Melbourne.Google Scholar
Yim, CY, Soczynska, JK, Kennedy, SH, Woldeyohannes, HO, Brietzke, E, McIntyre, RS (2012). The effect of overweight/obesity on cognitive function in euthymic individuals with bipolar disorder. European Psychiatry 27, 223228.Google Scholar
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429435.Google Scholar