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Whole-brain white matter abnormalities in human cocaine and heroin use disorders: association with craving, recency, and cumulative use

Molecular Psychiatry volume 28, pages 780–791 (2023)Cite this article

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Abstract

Neuroimaging studies in substance use disorder have shown widespread impairments in white matter (WM) microstructure suggesting demyelination and axonal damage. However, substantially fewer studies explored the generalized vs. the acute and/or specific drug effects on WM. Our study assessed whole-brain WM integrity in three subgroups of individuals addicted to drugs, encompassing those with cocaine (CUD) or heroin (HUD) use disorder, compared to healthy controls (CTL). Diffusion MRI was acquired in 58 CTL, 28 current cocaine users/CUD+, 32 abstinent cocaine users/CUD−, and 30 individuals with HUD (urine was positive for cocaine in CUD+ and opiates used for treatment in HUD). Tract-Based Spatial Statistics allowed voxelwise analyses of diffusion metrics [fractional anisotropy (FA), mean diffusivity (MD), radial diffusivity (RD), and axial diffusivity (AD)]. Permutation statistics (p-corrected < 0.05) were used for between-group t-tests. Compared to CTL, all individuals with addiction showed widespread decreases in FA, and increases in MD, RD, and AD (19–57% of WM skeleton, p < 0.05). The HUD group showed the most impairments, followed by the CUD+, with only minor FA reductions in CUD− (<0.2% of WM skeleton, p = 0.05). Longer periods of regular use were associated with decreased FA and AD, and higher subjective craving was associated with increased MD, RD, and AD, across all individuals with drug addiction (p < 0.05). These findings demonstrate extensive WM impairments in individuals with drug addiction characterized by decreased anisotropy and increased diffusivity, thought to reflect demyelination and lower axonal packing. Extensive abnormalities in both groups with positive urine status (CUD+ and HUD), and correlations with craving, suggest greater WM impairments with more recent use. Results in CUD−, and correlations with regular use, further imply cumulative and/or persistent WM damage.

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Fig. 1: Whole-brain differences between healthy controls (CTL) and individuals with substance use disorder (SUD).
Fig. 2: Group-specific whole-brain differences of fractional anisotropy (FA) and mean diffusivities (MD).
Fig. 3: Group-specific whole-brain differences of axial (AD) and radial diffusivities (RD).
Fig. 4: Significant whole-brain voxelwise correlations between drug use variables and white matter (WM) diffusion metrics in individuals with SUD.

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Acknowledgements

This work was supported by the National Institute on Drug Abuse (Goldstein, 1R01DA048301-01A1), the National Center for Complementary and Integrative Health (Goldstein, 1R01AT010627-01), and the Canadian Institutes of Health Research (Gaudreault, postdoctoral research fellowship).

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  1. Psychiatry and Neuroscience Departments, Icahn School of Medicine at Mount Sinai, New York City, NY, USA

    Pierre-Olivier Gaudreault, Sarah G. King, Pias Malaker, Nelly Alia-Klein & Rita Z. Goldstein

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Study design: POG, NAK, RZG. Data management: PM. Data analysis: POG, SGK. Initial Manuscript writing: POG. Manuscript review: POG, SGK, PM, NAK, RZG.

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Correspondence to Rita Z. Goldstein.

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Gaudreault, PO., King, S.G., Malaker, P. et al. Whole-brain white matter abnormalities in human cocaine and heroin use disorders: association with craving, recency, and cumulative use. Mol Psychiatry 28, 780–791 (2023). https://doi.org/10.1038/s41380-022-01833-y

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