Altered White Matter Connectivity in Young Acutely Underweight Patients With Anorexia Nervosa

Daniel Geisler; Joseph A. King; Klaas Bahnsen; Fabio Bernardoni; Arne Doose; Dirk K. Müller; Michael Marxen; Veit Roessner; Martijn van den Heuvel; Stefan Ehrlich

doi:10.1016/j.jaac.2021.04.019

Altered White Matter Connectivity in Young Acutely Underweight Patients With Anorexia Nervosa

Daniel Geisler, Joseph A. King, Klaas Bahnsen, Fabio Bernardoni, Arne Doose, Dirk K. Müller, Michael Marxen, Veit Roessner, Martijn van den Heuvel, Stefan Ehrlich^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

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Abstract

Objective: Reductions of gray matter volume and cortical thickness in anorexia nervosa (AN) are well documented. However, findings regarding the integrity of white matter (WM) as studied via diffusion weighted imaging (DWI) are remarkably heterogeneous, and WM connectivity has been examined only in small samples using a limited number of regions of interest. The present study investigated whole-brain WM connectivity for the first time in a large sample of acutely underweight patients with AN. Method: DWI data from predominantly adolescent patients with acute AN (n = 96, mean age = 16.3 years) and age-matched healthy control participants (n = 96, mean age = 17.2 years) were analyzed. WM connectivity networks were generated from fiber-tractography−derived streamlines connecting 233 cortical/subcortical regions. To identify group differences, network-based statistic was used while taking head motion, WM, and ventricular volume into account. Results: Patients with AN were characterized by 6 WM subnetworks with abnormal architecture, as indicated by increased fractional anisotropy located primarily in parietal−occipital regions and accompanied by reduced radial diffusivity. Group differences based on number of streamlines reached only nominal significance. Conclusion: Our study reveals pronounced alterations in the WM connectome in young patients with AN. In contrast to known reductions in gray matter in the acutely underweight state of AN, this pattern does not necessarily indicate a deterioration of the WM network. Future studies using advanced MRI sequences will have to clarify interrelations with axonal packing or myelination, and whether the changes should be considered a consequence of undernutrition or a vulnerability for developing or maintaining AN.

Original language	English
Pages (from-to)	331-340
Number of pages	10
Journal	Journal of the American Academy of Child and Adolescent Psychiatry
Volume	61
Issue number	2
Early online date	11 May 2021
DOIs	https://doi.org/10.1016/j.jaac.2021.04.019
Publication status	Published - Feb 2022

Bibliographical note

Funding Information:
This work was supported by the Deutsche Forschungsgemeinschaft (EH 367/5-1, EH 367/7-1, SFB 940/2), the Swiss Anorexia Nervosa Foundation, the Marga und Walter Boll-Stiftung , and the B. Braun-Stiftung.

Funding Information:
This work was supported by the Deutsche Forschungsgemeinschaft (EH 367/5-1, EH 367/7-1, SFB 940/2), the Swiss Anorexia Nervosa Foundation, the Marga und Walter Boll-Stiftung, and the B. Braun-Stiftung.Disclosure: Prof. Dr. Roessner has received payment for consulting and writing activities from Eli Lilly and Co., Novartis, and Shire Pharmaceuticals/Takeda, lecture honoraria from Eli Lilly and Co., Novartis, Shire Pharmaceuticals/Takeda, and Medice Pharma, and support for research from Shire Pharmaceuticals/Takeda and Novartis. He has carried out (and is currently carrying out) clinical trials in cooperation with Novartis, Shire Pharmaceuticals/Takeda, Servier, and Otsuka. He has reported no financial relationship with the organizations that sponsored the research. Drs. King, Bernardoni, Marxen, Prof. Drs. van den Heuvel and Ehrlich, and Messrs. Geisler, Bahnsen, Doose, and M?ller have reported no biomedical financial interests or potential conflicts of interest. Author Contributions Conceptualization: Geisler, van den Heuvel, Ehrlich Data curation: Geisler, Bernardoni, Doose, M?ller Formal analysis: Geisler, Bernardoni Funding acquisition: Ehrlich Investigation: Geisler, King, Bahnsen, Bernardoni, Doose Methodology: M?ller, van den Heuvel, Ehrlich Project administration: King, Ehrlich Resources: M?ller, Marxen, Roessner, van den Heuvel, Ehrlich Software: Geisler, Bernardoni, van den Heuvel Supervision: van den Heuvel, Ehrlich Validation: van den Heuvel, Ehrlich Visualization: Geisler Writing ? original draft: Geisler, Ehrlich Writing ? review and editing: Geisler, King, Bahnsen, Bernardoni, Doose, M?ller, Marxen, Roessner, van den Heuvel, Ehrlich

Publisher Copyright:
© 2021 American Academy of Child and Adolescent Psychiatry

Keywords

anorexia nervosa
diffusion weighted imaging
fiber tractography
structural connectivity
white matter

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Altered White Matter Connectivity in Young Acutely Underweight Patients With Anorexia NervosaFinal published version, 1.1 MBLicence: Article 25fa Dutch Copyright Act

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Geisler, D., King, J. A., Bahnsen, K., Bernardoni, F., Doose, A., Müller, D. K., Marxen, M., Roessner, V., van den Heuvel, M., & Ehrlich, S. (2022). Altered White Matter Connectivity in Young Acutely Underweight Patients With Anorexia Nervosa. Journal of the American Academy of Child and Adolescent Psychiatry, 61(2), 331-340. https://doi.org/10.1016/j.jaac.2021.04.019

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abstract = "Objective: Reductions of gray matter volume and cortical thickness in anorexia nervosa (AN) are well documented. However, findings regarding the integrity of white matter (WM) as studied via diffusion weighted imaging (DWI) are remarkably heterogeneous, and WM connectivity has been examined only in small samples using a limited number of regions of interest. The present study investigated whole-brain WM connectivity for the first time in a large sample of acutely underweight patients with AN. Method: DWI data from predominantly adolescent patients with acute AN (n = 96, mean age = 16.3 years) and age-matched healthy control participants (n = 96, mean age = 17.2 years) were analyzed. WM connectivity networks were generated from fiber-tractography−derived streamlines connecting 233 cortical/subcortical regions. To identify group differences, network-based statistic was used while taking head motion, WM, and ventricular volume into account. Results: Patients with AN were characterized by 6 WM subnetworks with abnormal architecture, as indicated by increased fractional anisotropy located primarily in parietal−occipital regions and accompanied by reduced radial diffusivity. Group differences based on number of streamlines reached only nominal significance. Conclusion: Our study reveals pronounced alterations in the WM connectome in young patients with AN. In contrast to known reductions in gray matter in the acutely underweight state of AN, this pattern does not necessarily indicate a deterioration of the WM network. Future studies using advanced MRI sequences will have to clarify interrelations with axonal packing or myelination, and whether the changes should be considered a consequence of undernutrition or a vulnerability for developing or maintaining AN.",

keywords = "anorexia nervosa, diffusion weighted imaging, fiber tractography, structural connectivity, white matter",

author = "Daniel Geisler and King, {Joseph A.} and Klaas Bahnsen and Fabio Bernardoni and Arne Doose and M{\"u}ller, {Dirk K.} and Michael Marxen and Veit Roessner and {van den Heuvel}, Martijn and Stefan Ehrlich",

note = "Funding Information: This work was supported by the Deutsche Forschungsgemeinschaft (EH 367/5-1, EH 367/7-1, SFB 940/2), the Swiss Anorexia Nervosa Foundation, the Marga und Walter Boll-Stiftung , and the B. Braun-Stiftung. Funding Information: This work was supported by the Deutsche Forschungsgemeinschaft (EH 367/5-1, EH 367/7-1, SFB 940/2), the Swiss Anorexia Nervosa Foundation, the Marga und Walter Boll-Stiftung, and the B. Braun-Stiftung.Disclosure: Prof. Dr. Roessner has received payment for consulting and writing activities from Eli Lilly and Co., Novartis, and Shire Pharmaceuticals/Takeda, lecture honoraria from Eli Lilly and Co., Novartis, Shire Pharmaceuticals/Takeda, and Medice Pharma, and support for research from Shire Pharmaceuticals/Takeda and Novartis. He has carried out (and is currently carrying out) clinical trials in cooperation with Novartis, Shire Pharmaceuticals/Takeda, Servier, and Otsuka. He has reported no financial relationship with the organizations that sponsored the research. Drs. King, Bernardoni, Marxen, Prof. Drs. van den Heuvel and Ehrlich, and Messrs. Geisler, Bahnsen, Doose, and M?ller have reported no biomedical financial interests or potential conflicts of interest. Author Contributions Conceptualization: Geisler, van den Heuvel, Ehrlich Data curation: Geisler, Bernardoni, Doose, M?ller Formal analysis: Geisler, Bernardoni Funding acquisition: Ehrlich Investigation: Geisler, King, Bahnsen, Bernardoni, Doose Methodology: M?ller, van den Heuvel, Ehrlich Project administration: King, Ehrlich Resources: M?ller, Marxen, Roessner, van den Heuvel, Ehrlich Software: Geisler, Bernardoni, van den Heuvel Supervision: van den Heuvel, Ehrlich Validation: van den Heuvel, Ehrlich Visualization: Geisler Writing ? original draft: Geisler, Ehrlich Writing ? review and editing: Geisler, King, Bahnsen, Bernardoni, Doose, M?ller, Marxen, Roessner, van den Heuvel, Ehrlich Publisher Copyright: {\textcopyright} 2021 American Academy of Child and Adolescent Psychiatry",

year = "2022",

month = feb,

doi = "10.1016/j.jaac.2021.04.019",

language = "English",

volume = "61",

pages = "331--340",

journal = "Journal of the American Academy of Child and Adolescent Psychiatry",

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T1 - Altered White Matter Connectivity in Young Acutely Underweight Patients With Anorexia Nervosa

AU - Geisler, Daniel

AU - King, Joseph A.

AU - Bahnsen, Klaas

AU - Bernardoni, Fabio

AU - Doose, Arne

AU - Müller, Dirk K.

AU - Marxen, Michael

AU - Roessner, Veit

AU - van den Heuvel, Martijn

AU - Ehrlich, Stefan

N1 - Funding Information: This work was supported by the Deutsche Forschungsgemeinschaft (EH 367/5-1, EH 367/7-1, SFB 940/2), the Swiss Anorexia Nervosa Foundation, the Marga und Walter Boll-Stiftung , and the B. Braun-Stiftung. Funding Information: This work was supported by the Deutsche Forschungsgemeinschaft (EH 367/5-1, EH 367/7-1, SFB 940/2), the Swiss Anorexia Nervosa Foundation, the Marga und Walter Boll-Stiftung, and the B. Braun-Stiftung.Disclosure: Prof. Dr. Roessner has received payment for consulting and writing activities from Eli Lilly and Co., Novartis, and Shire Pharmaceuticals/Takeda, lecture honoraria from Eli Lilly and Co., Novartis, Shire Pharmaceuticals/Takeda, and Medice Pharma, and support for research from Shire Pharmaceuticals/Takeda and Novartis. He has carried out (and is currently carrying out) clinical trials in cooperation with Novartis, Shire Pharmaceuticals/Takeda, Servier, and Otsuka. He has reported no financial relationship with the organizations that sponsored the research. Drs. King, Bernardoni, Marxen, Prof. Drs. van den Heuvel and Ehrlich, and Messrs. Geisler, Bahnsen, Doose, and M?ller have reported no biomedical financial interests or potential conflicts of interest. Author Contributions Conceptualization: Geisler, van den Heuvel, Ehrlich Data curation: Geisler, Bernardoni, Doose, M?ller Formal analysis: Geisler, Bernardoni Funding acquisition: Ehrlich Investigation: Geisler, King, Bahnsen, Bernardoni, Doose Methodology: M?ller, van den Heuvel, Ehrlich Project administration: King, Ehrlich Resources: M?ller, Marxen, Roessner, van den Heuvel, Ehrlich Software: Geisler, Bernardoni, van den Heuvel Supervision: van den Heuvel, Ehrlich Validation: van den Heuvel, Ehrlich Visualization: Geisler Writing ? original draft: Geisler, Ehrlich Writing ? review and editing: Geisler, King, Bahnsen, Bernardoni, Doose, M?ller, Marxen, Roessner, van den Heuvel, Ehrlich Publisher Copyright: © 2021 American Academy of Child and Adolescent Psychiatry

PY - 2022/2

Y1 - 2022/2

N2 - Objective: Reductions of gray matter volume and cortical thickness in anorexia nervosa (AN) are well documented. However, findings regarding the integrity of white matter (WM) as studied via diffusion weighted imaging (DWI) are remarkably heterogeneous, and WM connectivity has been examined only in small samples using a limited number of regions of interest. The present study investigated whole-brain WM connectivity for the first time in a large sample of acutely underweight patients with AN. Method: DWI data from predominantly adolescent patients with acute AN (n = 96, mean age = 16.3 years) and age-matched healthy control participants (n = 96, mean age = 17.2 years) were analyzed. WM connectivity networks were generated from fiber-tractography−derived streamlines connecting 233 cortical/subcortical regions. To identify group differences, network-based statistic was used while taking head motion, WM, and ventricular volume into account. Results: Patients with AN were characterized by 6 WM subnetworks with abnormal architecture, as indicated by increased fractional anisotropy located primarily in parietal−occipital regions and accompanied by reduced radial diffusivity. Group differences based on number of streamlines reached only nominal significance. Conclusion: Our study reveals pronounced alterations in the WM connectome in young patients with AN. In contrast to known reductions in gray matter in the acutely underweight state of AN, this pattern does not necessarily indicate a deterioration of the WM network. Future studies using advanced MRI sequences will have to clarify interrelations with axonal packing or myelination, and whether the changes should be considered a consequence of undernutrition or a vulnerability for developing or maintaining AN.

AB - Objective: Reductions of gray matter volume and cortical thickness in anorexia nervosa (AN) are well documented. However, findings regarding the integrity of white matter (WM) as studied via diffusion weighted imaging (DWI) are remarkably heterogeneous, and WM connectivity has been examined only in small samples using a limited number of regions of interest. The present study investigated whole-brain WM connectivity for the first time in a large sample of acutely underweight patients with AN. Method: DWI data from predominantly adolescent patients with acute AN (n = 96, mean age = 16.3 years) and age-matched healthy control participants (n = 96, mean age = 17.2 years) were analyzed. WM connectivity networks were generated from fiber-tractography−derived streamlines connecting 233 cortical/subcortical regions. To identify group differences, network-based statistic was used while taking head motion, WM, and ventricular volume into account. Results: Patients with AN were characterized by 6 WM subnetworks with abnormal architecture, as indicated by increased fractional anisotropy located primarily in parietal−occipital regions and accompanied by reduced radial diffusivity. Group differences based on number of streamlines reached only nominal significance. Conclusion: Our study reveals pronounced alterations in the WM connectome in young patients with AN. In contrast to known reductions in gray matter in the acutely underweight state of AN, this pattern does not necessarily indicate a deterioration of the WM network. Future studies using advanced MRI sequences will have to clarify interrelations with axonal packing or myelination, and whether the changes should be considered a consequence of undernutrition or a vulnerability for developing or maintaining AN.

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Altered White Matter Connectivity in Young Acutely Underweight Patients With Anorexia Nervosa

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Bibliographical note

Keywords

UN SDGs

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