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Assessment of brain connectome alterations in male chronic smokers using structural and generalized q-sampling MRI

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Abstract

An association has been shown between chronic cigarette smoking and structural abnormalities in the brain areas related to several functions relevant to addictive behavior. However, few studies have focused on the structural alternations of chronic smoking by using magnetic resonance imaging (MRI). Also, it remains unclear how structural alternations are associated with tobacco-dependence severity and the positive/negative outcome expectances. The q-sampling imaging (GQI) is an advanced diffusion MRI technique that can reconstruct more precise and consistent images of complex oriented fibers than other methods. We aimed to use GQI to evaluate the impact of the neurological structure caused by chronic smoking. Sixty-seven chronic smokers and 43 nonsmokers underwent a MRI scan. The tobacco dependence severity and the positive/negative outcome expectancies were assessed via self-report. We used GQI with voxel-based statistical analysis (VBA) to evaluate structural brain and connectivity abnormalities. Graph theoretical analysis (GTA) and network-based statistical (NBS) analysis were also performed to identify the structural network differences among groups. Chronic smokers had smaller GM and WM volumes in the bilateral frontal lobe and bilateral frontal region. The GM/WM volumes correlated with dependence severity and outcome expectancies in the brain areas involving high-level functions. Chronic smokers had shape changes in the left hippocampal head and tail and the inferior brain stem. Poorer WM integrity in chronic smokers was found in the left middle frontal region, the right superior fronto-occipital fasciculus, the right temporal region, the left parahippocampus, the left anterior internal capsule, and the right inferior parietal region. WM integrity correlated with dependence severity and outcome expectancies in brain areas involving high-level functions. Chronic smokers had decreased local segregation and global integration among the brain regions and networks. Our results provide further evidence indicating that chronic smoking may be associated with brain structure and connectivity changes.

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Availability of data and materials

The datasets presented in this article are not readily available because the ethical approval and requirements of the data protection legislation. The data set will only be made available on a restricted basis according to the data sharing policies at Chang Gung University and Chung Shan Medical University Hospital. Requests to access the datasets should be directed to Jun-Cheng Weng, jcweng@mail.cgu.edu.tw.

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Funding

This study was supported by the research program MOST105-2410-H-040-001-MY3 and MOST110-2221-E-182-027, which were sponsored by the Ministry of Science and Technology, Taipei, Taiwan. This study was also supported by grants NMRPD1L0311of Chang Gung University, Taoyuan, Taiwan. The funders had no role in the conduct of the study nor the collection, analysis, and interpretation of data.

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Authors and Affiliations

  1. Department of Medical Imaging and Radiological Sciences, Graduate Institute of Artificial Intelligence, Chang Gung University, 33302, Taoyuan, Taiwan

    Jun-Cheng Weng, Yu-Chen Chuang & Li-Bang Zheng

  2. Medical Imaging Research Center, Institute for Radiological Research, Chang Gung University, Chang Gung Memorial Hospital at Linkou, 33302, Taoyuan, Taiwan

    Jun-Cheng Weng

  3. Department of Psychiatry, Chang Gung Memorial Hospital, 61363, Chiayi, Taiwan

    Jun-Cheng Weng

  4. Institute of Medical Device and Imaging, National Taiwan University College of Medicine, 10051, Taipei, Taiwan

    Yu-Chen Chuang

  5. Department of Medical Laboratory and Biotechnology, Chung Shan Medical University, 40201, Taichung, Taiwan

    Ming-Shih Lee

  6. Clinical Laboratory, Chung Shan Medical University Hospital, 40201, Taichung, Taiwan

    Ming-Shih Lee

  7. Department of Psychology, Chung Shan Medical University, 40201, Taichung, Taiwan

    Ming-Chou Ho

  8. Clinical Psychological Room, Chung Shan Medical University Hospital, 40201, Taichung, Taiwan

    Ming-Chou Ho

  9. Department of Psychology, Chung Shan Medical University, No.110, Sec. 1, Chien-Kuo N. Road, 402, Taichung, Taiwan

    Ming-Chou Ho

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  1. Jun-Cheng Weng
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Contributions

Conceptualization, M-C. H. and J-C. W.; methodology, J-C. W. and M-C. H.; software, Y-C. C. and L-B. Z.; validation, J-C. W.; formal analysis, Y-C. C. and L-B. Z.; investigation, M-C. H. and J-C. W.; resources, M-C. H. and M-S. L.; data curation, M-C. H. and M-S. L.; writing—original draft preparation, M-C. H. and J-C. W.; writing—review and editing, M-S. L.; visualization, Y-C. C. and L-B. Z.; supervision, J-C. W.; project administration, M-C. H. and J-C. W.; funding acquisition, M-C. H. and J-C. W. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Ming-Chou Ho.

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Ethical approval

This research was approved by the institutional review board of Chung Shan Medical University Hospital (CMUH No: CS2-14059). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

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Weng, JC., Chuang, YC., Zheng, LB. et al. Assessment of brain connectome alterations in male chronic smokers using structural and generalized q-sampling MRI. Brain Imaging and Behavior 16, 1761–1775 (2022). https://doi.org/10.1007/s11682-022-00647-4

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