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Interactions between overweight/obesity and alcohol dependence impact human brain white matter microstructure: evidence from DTI

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Abstract

There is inconsistent evidence for an association of obesity with white matter microstructural alterations. Such inconsistent findings may be related to the cumulative effects of obesity and alcohol dependence. This study aimed to investigate the possible interactions between alcohol dependence and overweight/obesity on white matter microstructure in the human brain. A total of 60 inpatients with alcohol dependence during early abstinence (44 normal weight and 16 overweight/obese) and 65 controls (42 normal weight and 23 overweight/obese) were included. The diffusion tensor imaging (DTI) measures [fractional anisotropy (FA) and radial diffusivity (RD)] of the white matter microstructure were compared between groups. We observed significant interactive effects between alcohol dependence and overweight/obesity on DTI measures in several tracts. The DTI measures were not significantly different between the overweight/obese and normal-weight groups (although widespread trends of increased FA and decreased RD were observed) among controls. However, among the alcohol-dependent patients, the overweight/obese group had widespread reductions in FA and widespread increases in RD, most of which significantly differed from the normal-weight group; among those with overweight/obesity, the alcohol-dependent group had widespread reductions in FA and widespread increases in RD, most of which were significantly different from the control group. This study found significant interactive effects between overweight/obesity and alcohol dependence on white matter microstructure, indicating that these two controllable factors may synergistically impact white matter microstructure and disrupt structural connectivity in the human brain.

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Data availability

The data that support the findings of this study are available from the corresponding author, Wan-jun Guo, upon reasonable request.

References

  1. Zorlu N, Gelal F, Kuserli A, Cenik E, Durmaz E, Saricicek A, Gulseren S (2013) Abnormal white matter integrity and decision-making deficits in alcohol dependence. Psychiatry Res 214:382–388

    Article  PubMed  Google Scholar 

  2. Pfefferbaum A, Rosenbloom MJ, Adalsteinsson E, Sullivan EV (2007) Diffusion tensor imaging with quantitative fibre tracking in hiv infection and alcoholism comorbidity: Synergistic white matter damage. Brain 130:48–64

    Article  PubMed  Google Scholar 

  3. Bagga D, Sharma A, Kumari A, Kaur P, Bhattacharya D, Garg ML, Khushu S, Singh N (2014) Decreased white matter integrity in fronto-occipital fasciculus bundles: Relation to visual information processing in alcohol-dependent subjects. Alcohol (Fayetteville, NY) 48:43–53

    Article  Google Scholar 

  4. Spindler C, Mallien L, Trautmann S, Alexander N, Muehlhan M (2022) A coordinate-based meta-analysis of white matter alterations in patients with alcohol use disorder. Transl Psychiatry 12:40

    Article  PubMed  PubMed Central  Google Scholar 

  5. Kullmann S, Schweizer F, Veit R, Fritsche A, Preissl H (2015) Compromised white matter integrity in obesity. Obesity Revi Off J Int Assoc Study Obesity 16:273–281

    Article  CAS  Google Scholar 

  6. 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 (Silver Spring) 19:500–504

    Article  PubMed  Google Scholar 

  7. Wang H, Wang J, Liu MM, Wang D, Liu YQ, Zhao Y, Huang MM, Liu Y, Sun J, Dong GH (2012) Epidemiology of general obesity, abdominal obesity and related risk factors in urban adults from 33 communities of northeast china: The chpsne study. BMC Public Health 12:967

    Article  PubMed  PubMed Central  Google Scholar 

  8. Jarvis CM, Hayman LL, Braun LT, Schwertz DW, Ferrans CE, Piano MR (2007) Cardiovascular risk factors and metabolic syndrome in alcohol- and nicotine-dependent men and women. J Cardiovasc Nurs 22:429–435

    Article  PubMed  Google Scholar 

  9. Koliaki C, Liatis S, Kokkinos A (2019) Obesity and cardiovascular disease: Revisiting an old relationship. Metabolism 92:98–107

    Article  PubMed  CAS  Google Scholar 

  10. Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX, Eckel RH (2006) Obesity and cardiovascular disease: Pathophysiology, evaluation, and effect of weight loss: An update of the 1997 american heart association scientific statement on obesity and heart disease from the obesity committee of the council on nutrition, physical activity, and metabolism. Circulation 113:898–918

    Article  PubMed  Google Scholar 

  11. Mokdad AH, Marks JS, Stroup DF, Gerberding JL (2004) Actual causes of death in the united states, 2000. JAMA 291:1238–1245

    Article  PubMed  Google Scholar 

  12. Raji CA, Ho AJ, Parikshak NN, Becker JT, Lopez OL, Kuller LH, Hua X, Leow AD, Toga AW, Thompson PM (2010) Brain structure and obesity. Hum Brain Mapp 31:353–364

    Article  PubMed  Google Scholar 

  13. Alfaro FJ, Gavrieli A, Saade-Lemus P, Lioutas VA, Upadhyay J, Novak V (2018) White matter microstructure and cognitive decline in metabolic syndrome: A review of diffusion tensor imaging. Metabolism 78:52–68

    Article  PubMed  CAS  Google Scholar 

  14. Shott ME, Cornier MA, Mittal VA, Pryor TL, Orr JM, Brown MS (2005) Frank GK (2015) Orbitofrontal cortex volume and brain reward response in obesity. Int J Obes 39:214–221

    Article  Google Scholar 

  15. Kullmann S, Callaghan MF, Heni M, Weiskopf N, Scheffler K, Häring HU, Fritsche A, Veit R, Preissl H (2016) Specific white matter tissue microstructure changes associated with obesity. Neuroimage 125:36–44

    Article  PubMed  Google Scholar 

  16. Ottino-González J, Jurado MA, García-García I, Segura B, Marqués-Iturria I, Sender-Palacios MJ, Tor E, Prats-Soteras X, Caldú X, Junqué C, Pasternak O, Garolera M (2018) Allostatic load and disordered white matter microstructure in overweight adults. Sci Rep 8:15898

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  17. Kuswanto CN, Sum MY, Yang GL, Nowinski WL, McIntyre RS, Sim K (2014) Increased body mass index makes an impact on brain white-matter integrity in adults with remitted first-episode mania. Psychol Med 44:533–541

    Article  PubMed  CAS  Google Scholar 

  18. Koivukangas J, Björnholm L, Tervonen O, Miettunen J, Nordström T, Kiviniemi V, Mäki P, Mukkala S, Moilanen I, Barnett JH, Jones PB, Nikkinen J, Veijola J (2016) Body mass index and brain white matter structure in young adults at risk for psychosis - the oulu brain and mind study. Psychiatry Res Neuroimaging 254:169–176

    Article  PubMed  Google Scholar 

  19. Rice J, Gu C (2019) Function and mechanism of myelin regulation in alcohol abuse and alcoholism. BioEssays News rev Mole Cell Develo Biol 41:e1800255

    Article  Google Scholar 

  20. Bouhrara M, Khattar N, Elango P, Resnick SM, Ferrucci L (2005) Spencer RG (2021) Evidence of association between obesity and lower cerebral myelin content in cognitively unimpaired adults. Int J Obes 45:850–859

    Article  Google Scholar 

  21. Chen Y, Pan Z, Meng F, Xu Q, Huang L, Pu X, Yu X, Wu Y, Lyu H, Lin X (2022) Assessment of rat sciatic nerve using diffusion-tensor imaging with readout-segmented echo planar imaging. Front Neurosci 16:938674

    Article  PubMed  PubMed Central  Google Scholar 

  22. Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15:435–455

    Article  PubMed  Google Scholar 

  23. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through mri as increased radial (but unchanged axial) diffusion of water. Neuroimage 17:1429–1436

    Article  PubMed  Google Scholar 

  24. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using dt-mri data. Magn Reson Med 44:625–632

    Article  PubMed  CAS  Google Scholar 

  25. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH (2003) Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20:1714–1722

    Article  PubMed  Google Scholar 

  26. Annett M (2004) Hand preference observed in large healthy samples: Classification, norms and interpretations of increased non-right-handedness by the right shift theory. Br J Psychol 95:339–353

    Article  PubMed  Google Scholar 

  27. Saunders JB, Aasland OG, Babor TF, de la Fuente JR, Grant M (1993) Development of the alcohol use disorders identification test (audit): Who collaborative project on early detection of persons with harmful alcohol consumption–ii. Addiction 88:791–804

    Article  PubMed  CAS  Google Scholar 

  28. World Health Organization (2016) The global status of overweight and obesity. In: Fact sheet. Geneva

  29. Cui Z, Zhong S, Xu P, He Y, Gong G (2013) Panda: A pipeline toolbox for analyzing brain diffusion images. Front Hum Neurosci 7:42

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  30. Volkow ND, Baler RD (2015) Now vs later brain circuits: Implications for obesity and addiction. Trends Neurosci 38:345–352

    Article  PubMed  CAS  Google Scholar 

  31. Volkow ND, Morales M (2015) The brain on drugs: From reward to addiction. Cell 162:712–725

    Article  PubMed  CAS  Google Scholar 

  32. Fortier CB, Leritz EC, Salat DH, Lindemer E, Maksimovskiy AL, Shepel J, Williams V, Venne JR, Milberg WP, McGlinchey RE (2014) Widespread effects of alcohol on white matter microstructure. Alcohol Clin Exp Res 38:2925–2933

    Article  PubMed  PubMed Central  Google Scholar 

  33. Wang L, Liu X, Luo X, Zeng M, Zuo L, Wang KS (2013) Genetic variants in the fat mass- and obesity-associated (fto) gene are associated with alcohol dependence. J Mol Neurosci 51:416–424

    Article  PubMed  CAS  Google Scholar 

  34. 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 (2010) A commonly carried allele of the obesity-related fto gene is associated with reduced brain volume in the healthy elderly. Proc Natl Acad Sci U S A 107:8404–8409

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  35. Dennis EL, Jahanshad N, Braskie MN, Warstadt NM, Hibar DP, Kohannim O, Nir TM, McMahon KL, de Zubicaray GI, Montgomery GW, Martin NG, Toga AW, Wright MJ, Thompson PM (2014) Obesity gene negr1 associated with white matter integrity in healthy young adults. Neuroimage 102(Pt 2):548–557

    Article  PubMed  CAS  Google Scholar 

  36. Wang KS, Zuo L, Pan Y, Xie C, Luo X (2015) Genetic variants in the cpne5 gene are associated with alcohol dependence and obesity in caucasian populations. J Psychiatr Res 71:1–7

    Article  PubMed  Google Scholar 

  37. Adams C, Conigrave JH, Lewohl J, Haber P, Morley KC (2020) Alcohol use disorder and circulating cytokines: A systematic review and meta-analysis. Brain Behav Immun 89:501–512

    Article  PubMed  CAS  Google Scholar 

  38. Das UN (2001) Is obesity an inflammatory condition? Nutrition 17:953–966

    Article  PubMed  CAS  Google Scholar 

  39. Levin SG, Godukhin OV (2017) Modulating effect of cytokines on mechanisms of synaptic plasticity in the brain. Biochemistry (Mosc) 82:264–274

    Article  PubMed  CAS  Google Scholar 

  40. Chen CH, Pan CH, Chen CC, Huang MC (2011) Increased oxidative DNA damage in patients with alcohol dependence and its correlation with alcohol withdrawal severity. Alcohol Clin Exp Res 35:338–344

    Article  PubMed  CAS  Google Scholar 

  41. Pérez-Torres I, Castrejón-Téllez V, Soto ME, Rubio-Ruiz ME, Manzano-Pech L, Guarner-Lans V (2021) Oxidative stress, plant natural antioxidants, and obesity. Int J Mol Sci 22

  42. Tobore TO (2020) Towards a comprehensive theory of obesity and a healthy diet: The causal role of oxidative stress in food addiction and obesity. Behav Brain Res 384:112560

    Article  PubMed  CAS  Google Scholar 

  43. 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. J Clin Endocrinol Metab 92:3278–3284

    Article  PubMed  CAS  Google Scholar 

  44. Mueller K, Möller HE, Horstmann A, Busse F, Lepsien J, Blüher M, Stumvoll M, Villringer A, Pleger B (2015) Physical exercise in overweight to obese individuals induces metabolic- and neurotrophic-related structural brain plasticity. Front Hum Neurosci 9:372

    Article  PubMed  PubMed Central  Google Scholar 

  45. Nota MHC, Vreeken D, Wiesmann M, Aarts EO, Hazebroek EJ, Kiliaan AJ (2020) Obesity affects brain structure and function- rescue by bariatric surgery? Neurosci Biobehav Rev 108:646–657

    Article  PubMed  Google Scholar 

  46. Tuulari JJ, Karlsson HK, Antikainen O, Hirvonen J, Pham T, Salminen P, Helmiö M, Parkkola R, Nuutila P, Nummenmaa L (2016) Bariatric surgery induces white and grey matter density recovery in the morbidly obese: A voxel-based morphometric study. Hum Brain Mapp 37:3745–3756

    Article  PubMed  PubMed Central  Google Scholar 

  47. Fritz M, Klawonn AM, Zahr NM (2022) Neuroimaging in alcohol use disorder: From mouse to man. J Neurosci Res 100:1140–1158

    Article  PubMed  CAS  Google Scholar 

  48. Alhassoon OM, Sorg SF, Taylor MJ, Stephan RA, Schweinsburg BC, Stricker NH, Gongvatana A, Grant I (2012) Callosal white matter microstructural recovery in abstinent alcoholics: A longitudinal diffusion tensor imaging study. Alcohol Clin Exp Res 36:1922–1931

    Article  PubMed  PubMed Central  Google Scholar 

  49. Gazdzinski S, Durazzo TC, Mon A, Yeh PH, Meyerhoff DJ (2010) Cerebral white matter recovery in abstinent alcoholics–a multimodality magnetic resonance study. Brain 133:1043–1053

    Article  PubMed  PubMed Central  Google Scholar 

  50. Roseribloom MJ, Pfefferbaum A, Sullivan EV (2004) Recovery of short-term memory and psychomotor speed but not postural stability with long-term sobriety in alcoholic women. Neuropsychology 18:589–597

    Article  PubMed  Google Scholar 

  51. Yao S, Song J, Gao L, Yan Y, Huang C, Ding H, Huang H, He Y, Sun R, Xu G (2015) Thalamocortical sensorimotor circuit damage associated with disorders of consciousness for diffuse axonal injury patients. J Neurol Sci 356:168–174

    Article  ADS  PubMed  Google Scholar 

  52. De Wilde B, Dom G, Hulstijn W, Sabbe B (2007) Motor functioning and alcohol dependence. Alcohol Clin Exp Res 31:1820–1825

    Article  PubMed  Google Scholar 

  53. Williams L, Jackson CP, Choe N, Pelland L, Scott SH, Reynolds JN (2014) Sensory-motor deficits in children with fetal alcohol spectrum disorder assessed using a robotic virtual reality platform. Alcohol Clin Exp Res 38:116–125

    Article  PubMed  Google Scholar 

  54. Monnig MA, Thayer RE, Caprihan A, Claus ED, Yeo RA, Calhoun VD, Hutchison KE (2014) White matter integrity is associated with alcohol cue reactivity in heavy drinkers. Brain Behav 4:158–170

    Article  PubMed  Google Scholar 

  55. Kullmann S, Abbas Z, Machann J, Shah NJ, Scheffler K, Birkenfeld AL, Häring HU, Fritsche A, Heni M, Preissl H (2020) Investigating obesity-associated brain inflammation using quantitative water content mapping. J Neuroendocrinol 32:e12907

    Article  PubMed  CAS  Google Scholar 

  56. Zhang Y, Ji G, Xu M, Cai W, Zhu Q, Qian L, Zhang YE, Yuan K, Liu J, Li Q, Cui G, Wang H, Zhao Q, Wu K, Fan D, Gold MS, Tian J, Tomasi D, Liu Y, Nie Y, Wang GJ (2016) Recovery of brain structural abnormalities in morbidly obese patients after bariatric surgery. Int J Obes (Lond) 40:1558–1565

    Article  PubMed  CAS  Google Scholar 

  57. Liao Y, Tang J, Deng Q, Deng Y, Luo T, Wang X, Chen H, Liu T, Chen X, Brody AL, Hao W (2011) Bilateral fronto-parietal integrity in young chronic cigarette smokers: A diffusion tensor imaging study. PLoS ONE 6:e26460

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  58. 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 6:e18544

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

We thank all individuals who participated in the study.

Funding

The study was partly supported by grants from the National Natural Science Foundation (grant no. 81571305 and 82171487) to Wan-jun Guo, and the Introduction Project of Suzhou Clinical Expert Team (grant no. SZYJTD201715) to Tao Li.

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Authors and Affiliations

  1. Mental Health Center, West China Hospital, Sichuan University, Chengdu, 610041, Sichuan, China

    Hai-Ling Cao, Ya-Jing Meng, Ren-Hao Deng, Ming-Li Li & Wan-Jun Guo

  2. Department of Neurobiology, Affiliated Mental Health Center and Hangzhou Seventh People’s Hospital, Zhejiang University School of Medicine, Hangzhou, 310063, China

    Wei Wei, Xiao-Jing Li, Wei Deng, Tao Li & Wan-Jun Guo

  3. Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-Machine Integration, State Key Laboratory of Brain-Machine Intelligence, Zhejiang University, 1369 West Wenyi Road, Hangzhou, 311121, China

    Wan-Jun Guo

  4. Department of Clinical Psychology, Suzhou Psychiatric Hospital, The Affiliated Guangji Hospital of Soochow University, Suzhou, Jiangsu, China

    Yan-Song Liu, Zhen Tang & Xiang-Dong Du

  5. Department of Psychiatry, University of Alberta, Edmonton, Canada

    Andrew J. Greenshaw

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  1. Hai-Ling Cao
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Contributions

WJG, TL, HLC designed the study and wrote the protocol. HLC, WW, YJM, RHD, XJL, WD contributed to data acquisition and resources. HLC undertook the statistical analysis with some help from WW and WJG. HLC wrote the first draft of the manuscript. YSL, ZT, XDD, TL and WJG contributed to funding acquisition. WJG, AJG and MLL contributed to the revision of the manuscript. All authors contributed to and approved the final manuscript.

Corresponding author

Correspondence to Wan-Jun Guo.

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Conflict of interests

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

The study was approved by the Ethics Committee of West China Hospital of Sichuan University.

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Informed consent was obtained from all participants included in the study.

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Cao, HL., Wei, W., Meng, YJ. et al. Interactions between overweight/obesity and alcohol dependence impact human brain white matter microstructure: evidence from DTI. Eur Arch Psychiatry Clin Neurosci (2024). https://doi.org/10.1007/s00406-024-01760-9

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