Effects of Adapted Physical Activity on White Matter Integrity in Patients with Schizophrenia

Overview

Journal Brain Sci

Publisher MDPI

Date 2024 Jul 27

PMID 39061450

Authors

Elise Leroux

Laura Masson

Maxime Trehout

Sonia Dollfus

Affiliations

Soon will be listed here.

Abstract

Schizophrenia is associated with changes in white matter (WM) integrity and with reduced life expectancy, in part because of the cardiometabolic side effects of antipsychotics. Physical activity (PA) has emerged as a candidate lifestyle intervention that is safe and effective. The study aimed to assess how an adapted PA program delivered remotely by web (e-APA) improved WM integrity in patients with schizophrenia (SZPs) and healthy controls (HCs) and to evaluate associations among WM integrity, cardiorespiratory fitness, and symptom severity. This longitudinal study was conducted over 16 weeks with 31 participants (18 SZPs and 13 HCs). Diffusion tensor imaging and tract-based spatial statistics were employed to assess WM integrity. Cardiorespiratory fitness was measured by maximal oxygen uptake (VOmax), and assessments for clinical symptoms included the Positive and Negative Syndrome Scale, Self-evaluation of Negative Symptoms and the Brief Negative Syndrome Scale (BNSS). Only the SZPs had significantly increased WM integrity after the e-APA program, with increased fractional anisotropy and decreased radial diffusivity in fasciculi involved in motor functions and language process. Furthermore, decreased negative symptoms assessed with BNSS were associated with greater WM integrity following the program. These findings suggest that e-APA may improve WM integrity abnormalities and support e-APA as a promising therapeutic strategy.

References

Leroux E, Delcroix N, Alary M, Razafimandimby A, Brazo P, Delamillieure P . Functional and white matter abnormalities in the language network in patients with schizophrenia: a combined study with diffusion tensor imaging and functional magnetic resonance imaging. Schizophr Res. 2013; 150(1):93-100. DOI: 10.1016/j.schres.2013.07.016. View

Reid M, White D, Kraguljac N, Lahti A . A combined diffusion tensor imaging and magnetic resonance spectroscopy study of patients with schizophrenia. Schizophr Res. 2016; 170(2-3):341-50. PMC: 5982513. DOI: 10.1016/j.schres.2015.12.003. View

Kirkpatrick B, Saoud J, Strauss G, Ahmed A, Tatsumi K, Opler M . The brief negative symptom scale (BNSS): Sensitivity to treatment effects. Schizophr Res. 2017; 197:269-273. DOI: 10.1016/j.schres.2017.11.031. View

Bashir S, Al-Sultan F, Jamea A, Almousa A, Alnafisah M, Alzahrani M . Physical exercise keeps the brain connected by increasing white matter integrity in healthy controls. Medicine (Baltimore). 2021; 100(35):e27015. PMC: 8415959. DOI: 10.1097/MD.0000000000027015. View

Herbet G, Zemmoura I, Duffau H . Functional Anatomy of the Inferior Longitudinal Fasciculus: From Historical Reports to Current Hypotheses. Front Neuroanat. 2018; 12:77. PMC: 6156142. DOI: 10.3389/fnana.2018.00077. View

Ellison-Wright I, Nathan P, Bullmore E, Zaman R, Dudas R, Agius M . Distribution of tract deficits in schizophrenia. BMC Psychiatry. 2014; 14:99. PMC: 4108049. DOI: 10.1186/1471-244X-14-99. View

Dietsche B, Kircher T, Falkenberg I . Structural brain changes in schizophrenia at different stages of the illness: A selective review of longitudinal magnetic resonance imaging studies. Aust N Z J Psychiatry. 2017; 51(5):500-508. DOI: 10.1177/0004867417699473. View

Makris N, Kennedy D, McInerney S, Sorensen A, Wang R, Caviness Jr V . Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb Cortex. 2004; 15(6):854-69. DOI: 10.1093/cercor/bhh186. View

Bartzokis G, Lu P, Nuechterlein K, Gitlin M, Doi C, Edwards N . Differential effects of typical and atypical antipsychotics on brain myelination in schizophrenia. Schizophr Res. 2007; 93(1-3):13-22. PMC: 1974878. DOI: 10.1016/j.schres.2007.02.011. View

10.

Leroux E, Poirel N, Dollfus S . Anatomical Connectivity of the Visuospatial Attentional Network in Schizophrenia: A Diffusion Tensor Imaging Tractography Study. J Neuropsychiatry Clin Neurosci. 2020; 32(3):266-273. DOI: 10.1176/appi.neuropsych.19040101. View

11.

Lee I, Skerrett P . Physical activity and all-cause mortality: what is the dose-response relation?. Med Sci Sports Exerc. 2001; 33(6 Suppl):S459-71; discussion S493-4. DOI: 10.1097/00005768-200106001-00016. View

12.

Singh R, Bansal Y, Medhi B, Kuhad A . Antipsychotics-induced metabolic alterations: Recounting the mechanistic insights, therapeutic targets and pharmacological alternatives. Eur J Pharmacol. 2018; 844:231-240. DOI: 10.1016/j.ejphar.2018.12.003. View

13.

Keefe R, Bilder R, Davis S, Harvey P, Palmer B, Gold J . Neurocognitive effects of antipsychotic medications in patients with chronic schizophrenia in the CATIE Trial. Arch Gen Psychiatry. 2007; 64(6):633-47. DOI: 10.1001/archpsyc.64.6.633. View

14.

Chen F, Soya H, Yassa M, Li R, Chu C, Chen A . Effects of exercise types on white matter microstructure in late midlife adults: Preliminary results from a diffusion tensor imaging study. Front Aging Neurosci. 2022; 14:943992. PMC: 9716128. DOI: 10.3389/fnagi.2022.943992. View

15.

Olabi B, Ellison-Wright I, McIntosh A, Wood S, Bullmore E, Lawrie S . Are there progressive brain changes in schizophrenia? A meta-analysis of structural magnetic resonance imaging studies. Biol Psychiatry. 2011; 70(1):88-96. DOI: 10.1016/j.biopsych.2011.01.032. View

16.

Loprinzi P, Harper J, Ikuta T . The effects of aerobic exercise on corpus callosum integrity: systematic review. Phys Sportsmed. 2020; 48(4):400-406. DOI: 10.1080/00913847.2020.1758545. View

17.

Alexander A, Lee J, Lazar M, Field A . Diffusion tensor imaging of the brain. Neurotherapeutics. 2007; 4(3):316-29. PMC: 2041910. DOI: 10.1016/j.nurt.2007.05.011. View

18.

Gurusamy J, Gandhi S, Damodharan D, Ganesan V, Palaniappan M . Exercise, diet and educational interventions for metabolic syndrome in persons with schizophrenia: A systematic review. Asian J Psychiatr. 2018; 36:73-85. DOI: 10.1016/j.ajp.2018.06.018. View

19.

Smith S, Nichols T . Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2008; 44(1):83-98. DOI: 10.1016/j.neuroimage.2008.03.061. View

20.

Galderisi S, Kaiser S, Bitter I, Nordentoft M, Mucci A, Sabe M . EPA guidance on treatment of negative symptoms in schizophrenia. Eur Psychiatry. 2021; 64(1):e21. PMC: 8057437. DOI: 10.1192/j.eurpsy.2021.13. View