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Structural connectivity changes in the cerebral pain matrix in burning mouth syndrome: a multi-shell, multi-tissue-constrained spherical deconvolution model analysis

  • Diagnostic Neuroradiology
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Abstract

Purpose

Burning mouth syndrome (BMS) is a chronic intraoral pain syndrome. Previous studies have attempted to determine the brain connectivity features in BMS using functional and structural magnetic resonance imaging. However, no study has investigated the structural connectivity using multi-shell, multi-tissue-constrained spherical deconvolution (MSMT-CSD), anatomically constrained tractography (ACT), and spherical deconvolution informed filtering of tractograms (SIFT). Therefore, this study aimed to assess the differences in brain structural connectivity of patients with BMS and healthy controls using probabilistic tractography with these methods, and graph analysis.

Methods

Fourteen patients with BMS and 11 age- and sex-matched healthy volunteers underwent 3-T magnetic resonance imaging. MSMT-CSD-based probabilistic structural connectivity was computed using the second-order integration over fiber orientation distributions algorithm based on nodes set in 84 anatomical cortical regions with ACT and SIFT. A t-test was performed for comparisons between the BMS and healthy control brain networks.

Results

The betweenness centrality was significantly higher in the left insula, right amygdala, and right lateral orbitofrontal cortex and significantly lower in the right inferotemporal cortex in the BMS group than that in healthy controls. However, no significant difference was found in the clustering coefficient, node degree, and small-worldness between the two groups.

Conclusion

Graph analysis of brain probabilistic structural connectivity, based on diffusion imaging using an MSMT-CSD model with ACT and SIFT, revealed alterations in the regions comprising the pain matrix and medial pain ascending pathway. These results highlight the emotional-affective profile of BMS, which is a type of chronic pain syndrome.

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Data availability

Data cannot be shared publicly because of hospital regulations. Data are available from the University of Tokyo Hospital Institutional Data Access for researchers who meet the criteria for access to confidential data. Please contact the Graduate School of Medicine and Faculty of Medicine, The University of Tokyo Research Ethics Committee (ethics@m.u-tokyo.ac.jp) if you ask for our original data.

Abbreviations

5TT:

Five-tissue-type

ACT:

Anatomically constrained tractography

BC:

Betweenness centrality

BMS:

Burning mouth syndrome

CSD:

Constrained spherical deconvolution

EPI:

Echo planar imaging

iFOD2:

A second-order integration over fiber orientation distributions

MRI:

Magnetic resonance imaging

MSMT:

Multi-tissue-constrained spherical deconvolution

PTSD:

Post-traumatic stress disorder

ROI:

Region of interest

SIFT:

Spherical deconvolution informed filtering of tractograms

TE:

Echo time

TR:

Repetition time

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Acknowledgements

We appreciate Dr. Yoshiki Imamura (Department of Oral Diagnostic Sciences, Nihon University School of Dentistry, Tokyo, Japan) for his professional advice on burning mouth syndrome. We would like to thank Editage (http://www.editage.com) for editing and reviewing this manuscript for English language.

Funding

This work was supported by JSPS KAKENHI Grant Number 16K10330.

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Authors and Affiliations

  1. Department of Radiology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan

    Ryo Kurokawa, Kouhei Kamiya, Shohei Inui, Shimpei Kato, Fumio Suzuki, Shiori Amemiya & Osamu Abe

  2. Department of Radiology, Toho University, Tokyo, Japan

    Kouhei Kamiya

  3. Department of Oral Diagnostic Sciences, Nihon University School of Dentistry, Tokyo, Japan

    Takahiro Shinozaki & Daiki Takanezawa

  4. Department of Oral and Maxillofacial Radiology, Nihon University School of Dentistry, Tokyo, Japan

    Ryutarou Kohashi

Authors
  1. Ryo Kurokawa
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Contributions

Conceptualization: Ryo Kurokawa, Kouhei Kamiya, Shiori Amemiya, Osamu Abe. Data curation: Ryo Kurokawa, Shimpei Kato, Fumio Suzuki, Shiori Amemiya, Takahiro Shinozaki, Daiki Takanezawa, Ryutarou Kohashi, Osamu Abe. Methodology: Ryo Kurokawa, Kouhei Kamiya, Shiori Amemiya, Takahiro Shinozaki. Formal analysis and investigation: Ryo Kurokawa, Osamu Abe. Writing – original draft preparation: Ryo Kurokawa, Shohei Inui. Writing – review and editing: Kouhei Kamiya, Shimpei Kato, Fumio Suzuki, Shiori Amemiya. Funding acquisition: Osamu Abe. Resources: Takahiro Shinozaki, Daiki Takanezawa, Ryutarou Kohashi. Supervision: Osamu Abe.

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Correspondence to Ryo Kurokawa.

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We have a grant from Siemens Healthcare K.K.

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This multi-institutional prospective study was approved by the local ethics committees [IRB 11742, 2016–21] of the hospitals and performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

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Kurokawa, R., Kamiya, K., Inui, S. et al. Structural connectivity changes in the cerebral pain matrix in burning mouth syndrome: a multi-shell, multi-tissue-constrained spherical deconvolution model analysis. Neuroradiology 63, 2005–2012 (2021). https://doi.org/10.1007/s00234-021-02732-9

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