Corpus callosum morphology and relationships to illness phenotypes in individuals with anorexia nervosa.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
15 05 2024
Historique:
received: 10 11 2023
accepted: 10 05 2024
medline: 16 5 2024
pubmed: 16 5 2024
entrez: 15 5 2024
Statut: epublish

Résumé

Anorexia nervosa is an often-severe psychiatric illness characterized by significantly low body weight, fear of gaining weight, and distorted body image. Multiple neuroimaging studies have shown abnormalities in cortical morphology, mostly associated with the starvation state. Investigations of white matter, while more limited in number, have suggested global and regional volume reductions, as well as abnormal diffusivity in multiple regions including the corpus callosum. Yet, no study has specifically examined thickness of the corpus callosum, a large white matter tract instrumental in the inter-hemispheric integration of sensory, motor, and cognitive information. We analyzed MRI data from 48 adolescents and adults with anorexia nervosa and 50 healthy controls, all girls/women, to compare corpus callosum thickness and examined relationships with body mass index (BMI), illness duration, and eating disorder symptoms (controlling for BMI). There were no significant group differences in corpus callosum thickness. In the anorexia nervosa group, severity of body shape concerns was significantly, positively correlated with callosal thickness in the rostrum, genu, rostral body, isthmus, and splenium. In addition, there were significant positive correlations between eating disorder-related obsessions and compulsions and thickness of the anterior midbody, rostral body, and splenium. There were no significant associations between callosal thickness and BMI or illness duration. In sum, those with AN with worse concerns about bodily appearance and worse eating disorder-related obsessive thought patterns and compulsive behaviours have regionally thicker corpus callosum, independent of current weight status. These findings provide important neurobiological links to key, specific eating disorder behavioural phenotypes.

Identifiants

pubmed: 38750237
doi: 10.1038/s41598-024-61841-6
pii: 10.1038/s41598-024-61841-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

11112

Informations de copyright

© 2024. The Author(s).

Références

American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders 5th edn. (American Psychiatric Publishing, 2013).
doi: 10.1176/appi.books.9780890425596
Sullivan, P. F. Mortality in anorexia nervosa. Am. J. Psychiatry 152(7), 1073–1074 (1995).
pubmed: 7793446 doi: 10.1176/ajp.152.7.1073
Nickel, K. et al. Recovery of cortical volume and thickness after remission from acute anorexia nervosa. Int. J. Eat Disord. 51(9), 1056–1069 (2018).
pubmed: 30212599 doi: 10.1002/eat.22918
Walton, E. et al. Brain structure in acutely underweight and partially weight-restored individuals with anorexia nervosa: A coordinated analysis by the ENIGMA Eating Disorders Working Group. Biol. Psychiatry 92(9), 730–738 (2022).
pubmed: 36031441 doi: 10.1016/j.biopsych.2022.04.022
Reddy, P. V., Das, A. & Sastry, P. S. Quantitative and compositional changes in myelin of undernourished and protein malnourished rat brains. Brain Res. 161(2), 227–235 (1979).
pubmed: 215279 doi: 10.1016/0006-8993(79)90065-9
Chase, H. P., Dorsey, J. & McKhann, G. M. The effect of malnutrition on the synthesis of a myelin lipid. Pediatrics 40(4), 551–559 (1967).
pubmed: 6051054 doi: 10.1542/peds.40.4.551
Yusuf, H. K., Haque, Z. & Mozaffar, Z. Effect of malnutrition and subsequent rehabilitation on the development of mouse brain myelin. J. Neurochem. 36(3), 924–930 (1981).
pubmed: 7205282 doi: 10.1111/j.1471-4159.1981.tb01683.x
Wiggins, R. C. Myelin development and nutritional insufficiency. Brain Res. Rev. 4(2), 151–175 (1982).
doi: 10.1016/0165-0173(82)90016-9
Pappaianni, E. et al. Initial evidence of abnormal brain plasticity in anorexia nervosa: An ultra-high field study. Sci. Rep. 12(1), 2589 (2022).
pubmed: 35173174 pmcid: 8850617 doi: 10.1038/s41598-022-06113-x
Bomba, M. et al. Global and regional brain volumes normalization in weight-recovered adolescents with anorexia nervosa: Preliminary findings of a longitudinal voxel-based morphometry study. Neuropsychiatr. Dis. Treat. 11, 637–645 (2015).
pubmed: 25834442 pmcid: 4358418 doi: 10.2147/NDT.S73239
Katzman, D. K. et al. Cerebral gray matter and white matter volume deficits in adolescent girls with anorexia nervosa. J. Pediatr. 129(6), 794–803 (1996).
pubmed: 8969719 doi: 10.1016/S0022-3476(96)70021-5
Castro-Fornieles, J. et al. A cross-sectional and follow-up voxel-based morphometric MRI study in adolescent anorexia nervosa. J. Psychiatr. Res. 43(3), 331–340 (2009).
pubmed: 18486147 doi: 10.1016/j.jpsychires.2008.03.013
Asami, T. et al. Structural brain abnormalities in adolescent patients with anorexia nervosa at both the acute and weight-recovered phase. Brain Imaging Behav. 16(3), 1372–1380 (2022).
pubmed: 35025002 doi: 10.1007/s11682-021-00622-5
Katzman, D. K., Zipursky, R. B., Lambe, E. K. & Mikulis, D. J. A longitudinal magnetic resonance imaging study of brain changes in adolescents with anorexia nervosa. Arch. Pediatr. Adolesc. Med. 151(8), 793–797 (1997).
pubmed: 9265880 doi: 10.1001/archpedi.1997.02170450043006
Lázaro, L. et al. Normal gray and white matter volume after weight restoration in adolescents with anorexia nervosa. Int. J. Eat. Disord. 46(8), 841–848 (2013).
pubmed: 23904101 doi: 10.1002/eat.22161
Meneguzzo, P., Collantoni, E., Solmi, M., Tenconi, E. & Favaro, A. Anorexia nervosa and diffusion weighted imaging: An open methodological question raised by a systematic review and a fractional anisotropy anatomical likelihood estimation meta-analysis. Int. J. Eat. Disord. 52(11), 1237–1250 (2019).
pubmed: 31518016 doi: 10.1002/eat.23160
Barona, M. et al. White matter alterations in anorexia nervosa: Evidence from a voxel-based meta-analysis. Neurosci. Biobehav. Rev. 100, 285–295 (2019).
pubmed: 30851283 doi: 10.1016/j.neubiorev.2019.03.002
Zhang, S. et al. White matter abnormalities in anorexia nervosa: Psychoradiologic evidence from meta-analysis of diffusion tensor imaging studies using tract based spatial statistics. Front. Neurosci. 14, 159 (2020).
pubmed: 32194371 pmcid: 7063983 doi: 10.3389/fnins.2020.00159
Nickel, K. et al. White matter abnormalities in the corpus callosum in acute and recovered anorexia nervosa patients-a diffusion tensor imaging study. Front. Psychiatry 10, 490 (2019).
pubmed: 31338044 pmcid: 6628864 doi: 10.3389/fpsyt.2019.00490
Maier, S. et al. Reduced structural connectivity in the corpus callosum in patients with anorexia nervosa. Eur. Eat Disord. Rev. 30(4), 341–352 (2022).
pubmed: 35306728 doi: 10.1002/erv.2894
Geisler, D. et al. Altered white matter connectivity in young acutely underweight patients with anorexia nervosa. J. Am. Acad. Child Adolesc. Psychiatry 61(2), 331–340 (2022).
pubmed: 33989747 doi: 10.1016/j.jaac.2021.04.019
Lloyd, C. E. et al. Large-scale exploration of whole-brain structural connectivity in anorexia nervosa: Alterations in the connectivity of frontal and subcortical networks. Biol. Psychiatry Cogn. Neurosci. Neuroimag. 8(8), 864–873 (2023).
Schulte, T. & Müller-Oehring, E. M. Contribution of callosal connections to the interhemispheric integration of visuomotor and cognitive processes. Neuropsychol. Rev. 20(2), 174–190 (2010).
pubmed: 20411431 pmcid: 3442602 doi: 10.1007/s11065-010-9130-1
Witelson, S. F. Hand and sex differences in the isthmus and genu of the human corpus callosum. Brain 112(3), 799–835 (1989).
pubmed: 2731030 doi: 10.1093/brain/112.3.799
Filley, C. M. White matter: Organization and functional relevance. Neuropsychol. Rev. 20(2), 158–173 (2010).
pubmed: 20352350 doi: 10.1007/s11065-010-9127-9
Gazzaniga, M. S., Bogen, J. E. & Sperry, R. W. Observations on visual perception after disconnexion of the cerebral hemispheres in man. Brain 88(2), 221–236 (1965).
pubmed: 5828904 doi: 10.1093/brain/88.2.221
Treasure, J. et al. Anorexia nervosa. Nat. Rev. Dis. Primers 1, 15074 (2015).
pubmed: 27189821 doi: 10.1038/nrdp.2015.74
Gaudio, S. & Quattrocchi, C. C. Neural basis of a multidimensional model of body image distortion in anorexia nervosa. Neurosci. Biobehav. Rev. 36(8), 1839–1847 (2012).
pubmed: 22613629 doi: 10.1016/j.neubiorev.2012.05.003
Gaudio, S., Wiemerslage, L., Brooks, S. J. & Schiöth, H. B. A systematic review of resting-state functional-MRI studies in anorexia nervosa: Evidence for functional connectivity impairment in cognitive control and visuospatial and body-signal integration. Neurosci. Biobehav. Rev. 71, 578–589 (2016).
pubmed: 27725172 doi: 10.1016/j.neubiorev.2016.09.032
Stedal, K., Broomfield, C., Hay, P., Touyz, S. & Scherer, R. Neuropsychological functioning in adult anorexia nervosa: A meta-analysis. Neurosci. Biobehav. Rev. 130, 214–226 (2021).
pubmed: 34453951 doi: 10.1016/j.neubiorev.2021.08.021
Mölbert, S. C. et al. Depictive and metric body size estimation in anorexia nervosa and bulimia nervosa: A systematic review and meta-analysis. Clin. Psychol. Rev. 57, 21–31 (2017).
pubmed: 28818670 doi: 10.1016/j.cpr.2017.08.005
Godier, L. R. & Park, R. J. Compulsivity in anorexia nervosa: A transdiagnostic concept. Front. Psychol. 5, 778 (2014).
pubmed: 25101036 pmcid: 4101893 doi: 10.3389/fpsyg.2014.00778
Halmi, K. A. et al. Comorbidity of psychiatric diagnoses in anorexia nervosa. Arch. Gen. Psychiatry 48(8), 712–718 (1991).
pubmed: 1883254 doi: 10.1001/archpsyc.1991.01810320036006
Kaye, W. H., Bulik, C. M., Thornton, L., Barbarich, N. & Masters, K. Comorbidity of anxiety disorders with anorexia and bulimia nervosa. Am. J. Psychiatry 161(12), 2215–2221 (2004).
pubmed: 15569892 doi: 10.1176/appi.ajp.161.12.2215
Watson, H. J. et al. Genome-wide association study identifies eight risk loci and implicates metabo-psychiatric origins for anorexia nervosa. Nat. Genet. 51(8), 1207–1214 (2019).
pubmed: 31308545 pmcid: 6779477 doi: 10.1038/s41588-019-0439-2
Di Paola, M. et al. The structure of the corpus callosum in obsessive compulsive disorder. Eur. Psychiatry 28(8), 499–506 (2013).
pubmed: 23078960 doi: 10.1016/j.eurpsy.2012.07.001
Jose, D. et al. Corpus callosum abnormalities in medication-naïve adult patients with obsessive compulsive disorder. Psychiatry Res. 231(3), 341–345 (2015).
pubmed: 25686521 doi: 10.1016/j.pscychresns.2015.01.019
Luders, E., Thompson, P. M. & Kurth, F. Morphometry of the corpus callosum. In Brain Morphometry, Neuromethods (eds Spalletta, G. et al.) 131–142 (Springer, 2018).
Piras, F. et al. Corpus callosum morphology in major mental disorders: A magnetic resonance imaging study. Brain Commun. 3(2), fcab100 (2021).
pubmed: 34095833 pmcid: 8172496 doi: 10.1093/braincomms/fcab100
Freitag, C. M. et al. Total brain volume and corpus callosum size in medication-naïve adolescents and young adults with autism spectrum disorder. Biol. Psychiatry 66(4), 316–319 (2009).
pubmed: 19409535 pmcid: 3299337 doi: 10.1016/j.biopsych.2009.03.011
Tadayonnejad, R. et al. White matter tracts characteristics in habitual decision-making circuit underlie ritual behaviors in anorexia nervosa. Sci. Rep. 11(1), 15980 (2021).
pubmed: 34354139 pmcid: 8342714 doi: 10.1038/s41598-021-95300-3
Sheehan, D. V. et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): The Development and Validation of a Structured Diagnostic Psychiatric Interview for DSM-IV and ICD-10. J. Clin. Psychiatry 59(20), 22–33 (1998).
pubmed: 9881538
Sheehan, D. V. et al. Reliability and Validity of the Mini International Neuropsychiatric Interview for Children and Adolescents (MINI-KID). J. Clin. Psychiatry 71(3), 313–326 (2010).
pubmed: 20331933 doi: 10.4088/JCP.09m05305whi
Fairburn, C. G. & Cooper, Z. The Eating Disorder Examination. In Binge Eating: Nature, Assessment, and Treatment (eds Wilson, G. T. & Fairburn, C.) 317–360 (Guilford Press, 1993).
Mazure, C. M., Halmi, K. A., Sunday, S. R., Romano, S. J. & Einhorn, A. M. The Yale–Brown–Cornell eating disorder scale: Development, use, reliability and validity. J. Psychiatr. Res. 28(5), 425–445 (1994).
pubmed: 7897615 doi: 10.1016/0022-3956(94)90002-7
Hamilton, M. The assessment of anxiety states by rating. Br. J. Med. Psychol. 32(1), 50–55 (1959).
pubmed: 13638508 doi: 10.1111/j.2044-8341.1959.tb00467.x
Montgomery, S. A. & Åsberg, M. A new depression scale designed to be sensitive to change. Br. J. Psychiatry 134(4), 382–389 (1979).
pubmed: 444788 doi: 10.1192/bjp.134.4.382
Poznanski, E. O. & Mokros, H. B. Children’s Depression Rating Scale, Revised (CDRS-R) Manual (Western Psychological Services, 1996).
Carskadon, M. A. & Acebo, C. A self-administered rating scale for pubertal development. J. Adolesc. Health 14(3), 190–195 (1993).
pubmed: 8323929 doi: 10.1016/1054-139X(93)90004-9
Gaser, C., Dahnke, R., Thompson, P. M., Kurth, F., Luders, E. & Alzheimer’s Disease Neuroimaging Initiative. CAT—A computational anatomy toolbox for the analysis of structural MRI data. BioRxiv (2022).
Dale, C., Kalantary, D., Luders, E. & Kurth, F. Aberrant callosal morphology in ex-smokers. J. Integr. Neurosci. 21(4), 101 (2022).
pubmed: 35864753 doi: 10.31083/j.jin2104101
Simonsson, O. et al. Preliminary evidence of links between ayahuasca use and the corpus callosum. Front. Psychiatry 13, 1002455 (2022).
pubmed: 36386967 pmcid: 9643584 doi: 10.3389/fpsyt.2022.1002455
Luders, E. et al. Callosal morphology in Williams syndrome: A new evaluation of shape and thickness. Neuroreport 18(3), 203–207 (2007).
pubmed: 17314657 pmcid: 3197850 doi: 10.1097/WNR.0b013e3280115942
Luders, E. et al. The link between callosal thickness and intelligence in healthy children and adolescents. NeuroImage 54(3), 1823–1830 (2011).
pubmed: 20932920 doi: 10.1016/j.neuroimage.2010.09.083
Luders, E., Toga, A. W. & Thompson, P. M. Why size matters: Differences in brain volume account for apparent sex differences in callosal anatomy: The sexual dimorphism of the corpus callosum. NeuroImage 84, 820–824 (2014).
pubmed: 24064068 doi: 10.1016/j.neuroimage.2013.09.040
Luders, E. et al. Decreased callosal thickness in attention-deficit/hyperactivity disorder. Biol. Psychiatry 65(1), 84–88 (2009).
pubmed: 18842255 doi: 10.1016/j.biopsych.2008.08.027
Chavarria, M. C., Sánchez, F. J., Chou, Y. Y., Thompson, P. M. & Luders, E. Puberty in the corpus callosum. Neuroscience 265, 1–8 (2014).
pubmed: 24468104 doi: 10.1016/j.neuroscience.2014.01.030
Fabri, M., Pierpaoli, C., Barbaresi, P. & Polonara, G. Functional topography of the corpus callosum investigated by DTI and FMRI. World J. Radiol. 6(12), 895–906 (2014).
pubmed: 25550994 pmcid: 4278150 doi: 10.4329/wjr.v6.i12.895
Pierpaoli, C., Foschi, N., Fabri, M. & Polonara, G. Cortical activation during imitative behavior: An FMRI study in callosotomized patients. J. Syst. Integr. Neurosci. 7(3), 1–5 (2021).
doi: 10.15761/JSIN.1000253
Pierpaoli, C. et al. Imitation strategies in callosotomized patients. Arch. Ital. Biol. 156(1–2), 12–26 (2018).
pubmed: 30039832
Aboitiz, F. & Montiel, J. One hundred million years of interhemispheric communication: The history of the corpus callosum. Braz. J. Med. Biol. Res. 36(4), 409–420 (2003).
pubmed: 12700818 doi: 10.1590/S0100-879X2003000400002
Aboitiz, F., Scheibel, A. B., Fisher, R. S. & Zaidel, E. Fiber composition of the human corpus callosum. Brain Res. 598(1–2), 143–153 (1992).
pubmed: 1486477 doi: 10.1016/0006-8993(92)90178-C
Musiek, F. E. Neuroanatomy, neurophysiology, and central auditory assessment. Part III: Corpus callosum and efferent pathways. Ear Hear. 7(6), 349–358 (1986).
pubmed: 3792676 doi: 10.1097/00003446-198612000-00001
Goldstein, A., Covington, B. P., Mahabadi, N. & Mesfin, F. B. Neuroanatomy, Corpus Callosum [Internet] (StatPearls Publishing, 2023). https://www.ncbi.nlm.nih.gov/books/NBK448209/ [Updated 2023 Apr 3; cited 2023 Oct 8].
Schebendach, J. E. et al. Food choice and diet variety in weight-restored patients with anorexia nervosa. J. Am. Diet. Assoc. 111(5), 732. https://doi.org/10.1016/j.jada.2011.02.002 (2011).
doi: 10.1016/j.jada.2011.02.002 pubmed: 21515121 pmcid: 3083637
Sunday, S. R. & Halmi, K. A. Comparison of the Yale–Brown–Cornell eating disorders scale in recovered eating disorder patients, restrained dieters, and nondieting controls. Int. J. Eat. Disord. 28(4), 455–459 (2000).
pubmed: 11054794 doi: 10.1002/1098-108X(200012)28:4<455::AID-EAT15>3.0.CO;2-B

Auteurs

Jamie D Feusner (JD)

Centre for Addiction and Mental Health, 250 College St., Toronto, ON, M5T 1R8, Canada. jamie.feusner@utoronto.ca.
Department of Psychiatry, University of Toronto, Toronto, Canada. jamie.feusner@utoronto.ca.
Department of Women's and Children's Health, Karolinska Hospital, Karolinska Institutet, Stockholm, Sweden. jamie.feusner@utoronto.ca.
Department of Psychiatry and Biobehavioral Sciences, University of California Los Angeles, Los Angeles, CA, USA. jamie.feusner@utoronto.ca.

Alicja Nowacka (A)

School of Psychology, University of Auckland, Auckland, New Zealand.

Ronald Ly (R)

Department of Psychiatry and Biobehavioral Sciences, University of California Los Angeles, Los Angeles, CA, USA.

Eileen Luders (E)

School of Psychology, University of Auckland, Auckland, New Zealand.
Department of Women's and Children's Health, Uppsala University, Uppsala, Sweden.
Laboratory of Neuro Imaging, School of Medicine, University of Southern California, Los Angeles, CA, USA.

Florian Kurth (F)

School of Psychology, University of Auckland, Auckland, New Zealand.
Departments of Neuroradiology and Radiology, Jena University Hospital, Jena, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH