Cerebral Gray Matter Volume Changes in Patients with Neuropathic Pain from Total Brachial Plexus Injury

Clinical Neurology: Research Article

Wang J.a· Huang Z.b· Lu Y.c· Sha K.a· Li W.d· Zhao J.a

Author affiliations

aDepartment of Orthopaedics Trauma and Hand Surgery, First Affiliated Hospital of Guangxi Medical University, Nanning, China
bDepartment of Critical Care Medicine, The Second Affiliated Hospital of Guangxi Medical University, Nanning, China
cSichuan Cancer Hospital & Institute, Sichuan Cancer Center, Cancer Hospital Affiliate to School of Medicine, Chengdu, China
dDepartment of Radiology, First Affiliated Hospital of Guangxi Medical University, Nanning, China

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Article / Publication Details

Received: December 30, 2021
Accepted: June 08, 2022
Published online: July 28, 2022

Number of Print Pages: 10
Number of Figures: 2
Number of Tables: 3

ISSN: 0014-3022 (Print)
eISSN: 1421-9913 (Online)

For additional information: https://www.karger.com/ENE

Abstract

Introduction: Total brachial plexus injury not only significantly affects the motor and sensory function of the affected upper limbs but also causes further physical and mental damage to patients with long-term intractable pain. Previous studies mainly focused on the surgical treatment, while only a few paid attention to the intractable neuropathic pain caused by this injury. Changes in the volume of gray matter in the brain are thought to be associated with chronic neuropathic pain. Methods: Voxel-based morphometry analysis was used to compare the difference in cerebral gray matter volume between total brachial plexus injury patients with neuropathic pain and healthy controls. Correlations between pain duration, pain severity, and GM changes were analyzed. Results: The volume of cerebral gray matter in the patient group was decreased significantly in multiple regions, including the parahippocampal gyrus, paracentric lobule, inferior frontal gyrus, auxiliary motor cortex, middle occipital gyrus, right middle temporal gyrus, while it was increased in the insular, pons, middle frontal gyrus, cingulate gyrus, inferior parietal lobule, bilateral thalamus, and globus pallidus. There were no significant correlations between pain duration and rGMV changes, while a positive correlation was observed between pain severity and rGMV changes in one specific region, involving the anterior cingulate cortex. Conclusion: Total brachial plexus injury patients with chronic pain have widespread regions of gray matter atrophy and hypertrophy. The only positive correlation was observed between pain severity and rGMV changes in one specific region, suggesting that nociceptive stimuli trigger a variety of nonpain-specific processes, which confirms the multidimensional nature of pain.

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References Vranken JH. Mechanisms and treatment of neuropathic pain. Cent Nerv Syst Agents Med Chem. 2009 Mar;9(1):71–8. H Vranken J. Elucidation of pathophysiology and treatment of neuropathic pain. Cent Nerv Syst Agents Med Chem. 2012 Dec;12(4):304–14. Boadas-Vaello P, Castany S, Homs J, Álvarez-Pérez B, Deulofeu M, Verdú E. Neuroplasticity of ascending and descending pathways after somatosensory system injury: reviewing knowledge to identify neuropathic pain therapeutic targets. Spinal Cord. 2016 May;54(5):330–40. Serra-Blasco M, Portella MJ, Gómez-Ansón B, de Diego-Adeliño J, Vives-Gilabert Y, Puigdemont D, et al. Effects of illness duration and treatment resistance on grey matter abnormalities in major depression. Br J Psychiatry. 2013 Jun;202(6):434–40. Kucyi A, Davis KD. The dynamic pain connectome. Trends Neurosci. 2015 Feb;38(2):86–95. Kucyi A, Davis KD. The neural code for pain: from single-cell electrophysiology to the dynamic pain connectome. Neuroscientist. 2017 Aug;23(4):397–414. del Rey A, Apkarian AV, Martina M, Besedovsky HO. Chronic neuropathic pain-like behavior and brain-borne IL-1β. Ann N Y Acad Sci. 2012 Jul;1262(1):101–7. Yoon EJ, Kim YK, Shin HI, Lee Y, Kim SE. Cortical and white matter alterations in patients with neuropathic pain after spinal cord injury. Brain Res. 2013 Dec 2;1540:64–73. Sugimine S, Ogino Y, Kawamichi H, Obata H, Saito S. Brain morphological alternation in chronic pain patients with neuropathic characteristics. Mol Pain. 2016 Jun 8;12:174480691665240. Pan PL, Zhong JG, Shang HF, Zhu YL, Xiao PR, Dai ZY, et al. Quantitative meta-analysis of grey matter anomalies in neuropathic pain. Eur J Pain. 2015 Oct;19(9):1224–31. Eto K, Wake H, Watanabe M, Ishibashi H, Noda M, Yanagawa Y, et al. Inter-regional contribution of enhanced activity of the primary somatosensory cortex to the anterior cingulate cortex accelerates chronic pain behavior. J Neurosci. 2011 May 25;31(21):7631–6. Vierck CJ, Whitsel BL, Favorov OV, Brown AW, Tommerdahl M. Role of primary somatosensory cortex in the coding of pain. Pain. 2013 Mar;154(3):334–44. Stadler JA 3rd, Ellens DJ, Rosenow JM. Deep brain stimulation and motor cortical stimulation for neuropathic pain. Curr Pain Headache Rep. 2011 Feb;15(1):8–13. Flor H, Denke C, Schaefer M, Grüsser S. Effect of sensory discrimination training on cortical reorganisation and phantom limb pain. Lancet. 2001 Jun 2;357(9270):1763–4. Geha PY, Baliki MN, Harden RN, Bauer WR, Parrish TB, Apkarian AV. The brain in chronic CRPS pain: abnormal gray-white matter interactions in emotional and autonomic regions. Neuron. 2008 Nov 26;60(4):570–81. Barad MJ, Ueno T, Younger J, Chatterjee N, Mackey S. Complex regional pain syndrome is associated with structural abnormalities in pain-related regions of the human brain. J Pain. 2014 Feb;15(2):197–203. Kuchinad A, Schweinhardt P, Seminowicz DA, Wood PB, Chizh BA, Bushnell MC. Accelerated brain gray matter loss in fibromyalgia patients: premature aging of the brain? J Neurosci. 2007 Apr 11;27(15):4004–7. Niddam DM, Lee SH, Su YT, Chan RC. Brain structural changes in patients with chronic myofascial pain. Eur J Pain. 2017 Jan;21(1):148–58. Seminowicz DA, Davis KD. Pain enhances functional connectivity of a brain network evoked by performance of a cognitive task. J Neurophysiol. 2007 May;97(5):3651–9. Liu B, Li T, Tang WJ, Zhang JH, Sun HP, Xu WD, et al. Changes of inter-hemispheric functional connectivity between motor cortices after brachial plexuses injury: a resting-state fMRI study. Neuroscience. 2013 Jul 23;243:33–9. Lu Y, Liu H, Hua X, Xu WD, Xu JG, Gu YD. Supplementary motor cortical changes explored by resting-state functional connectivity in brachial plexus injury. World Neurosurg. 2016 Apr;88:300–5. Feng JT, Liu HQ, Hua XY, Gu YD, Xu JG, Xu WD. Brain functional network abnormality extends beyond the sensorimotor network in brachial plexus injury patients. Brain Imaging Behav. 2016 Dec;10(4):1198–205. Emerson NM, Zeidan F, Lobanov OV, Hadsel MS, Martucci KT, Quevedo AS, et al. Pain sensitivity is inversely related to regional grey matter density in the brain. Pain. 2014 Mar;155(3):566–73. Bhat DI, Indira Devi B, Bharti K, Panda R. Cortical plasticity after brachial plexus injury and repair: a resting-state functional MRI study. Neurosurg Focus. 2017 Mar;42(3):E14. Lu Y, Liu H, Hua X, Xu JG, Gu YD, Shen Y. Attenuation of brain grey matter volume in brachial plexus injury patients. Neurol Sci. 2016 Jan;37(1):51–6. Ashburner J, Friston KJ. Voxel-based morphometry: the methods. Neuroimage. 2000 Jun;11(6):805–21. Mutso AA, Petre B, Huang L, Baliki MN, Torbey S, Herrmann KM, et al. Reorganization of hippocampal functional connectivity with transition to chronic back pain. J Neurophysiol. 2014 Mar;111(5):1065–76. García-Larrea L, Peyron R, Mertens P, Gregoire CM, Lavenne F, Le Bars D, et al. Electrical stimulation of motor cortex for pain control: a combined PET-scan and electrophysiological study. Pain. 1999 Nov;83(2):259–73. MacIver K, Lloyd DM, Kelly S, Roberts N, Nurmikko T. Phantom limb pain, cortical reorganization and the therapeutic effect of mental imagery. Brain. 2008 Aug;131(8):2181–91. Alomar S, Bakhaidar M. Neuroimaging of neuropathic pain: review of current status and future directions. Neurosurg Rev. 2018 Jul;41(3):771–7. Broyd SJ, Demanuele C, Debener S, Helps SK, James CJ, Sonuga-Barke EJ. Default-mode brain dysfunction in mental disorders: a systematic review. Neurosci Biobehav Rev. 2009 Mar;33(3):279–96. Cauda F, Palermo S, Costa T, Torta R, Duca S, Vercelli U, et al. Gray matter alterations in chronic pain: a network-oriented meta-analytic approach. Neuroimage Clin. 2014 Apr 16;4:676–86. Ostrowsky K, Magnin M, Ryvlin P, Isnard J, Guenot M, Mauguière F. Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. Cereb Cortex. 2002 Apr;12(4):376–85. Sawamoto N, Honda M, Okada T, Hanakawa T, Kanda M, Fukuyama H, et al. Expectation of pain enhances responses to nonpainful somatosensory stimulation in the anterior cingulate cortex and parietal operculum/posterior insula: an event-related functional magnetic resonance imaging study. J Neurosci. 2000 Oct 1;20(19):7438–45. Zhang D, Raichle ME. Disease and the brain’s dark energy. Nat Rev Neurol. 2010 Jan;6(1):15–28. Moazen P, Torabi M, Azizi H, Fathollahi Y, Mirnajafi-Zadeh J, Semnanian S. The locus coeruleus noradrenergic system gates deficits in visual attention induced by chronic pain. Behav Brain Res. 2020 Jun 1;387:112600. Yoshizumi M, Parker RA, Eisenach JC, Hayashida K. Gabapentin inhibits γ-amino butyric acid release in the locus coeruleus but not in the spinal dorsal horn after peripheral nerve injury in rats. Anesthesiology. 2012 Jun;116(6):1347–53. Henderson LA, Peck CC, Petersen ET, Rae CD, Youssef AM, Reeves JM, et al. Chronic pain: lost inhibition? J Neurosci. 2013 Apr 24;33(17):7574–82. Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA. 1999 Dec 21;96(26):15222–7. Schmidt-Wilcke T, Leinisch E, Gänbauer S, Draganski B, Bogdahn U, Altmeppen J, et al. Affective components and intensity of pain correlate with structural differences in gray matter in chronic back pain patients. Pain. 2006 Nov;125(1):89–97. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain. 2005 Aug;9(4):463. Tsuda M, Koga K, Chen T, Zhuo M. Neuronal and microglial mechanisms for neuropathic pain in the spinal dorsal horn and anterior cingulate cortex. J Neurochem. 2017 May;141(4):486–98. Article / Publication Details

Received: December 30, 2021
Accepted: June 08, 2022
Published online: July 28, 2022

Number of Print Pages: 10
Number of Figures: 2
Number of Tables: 3

ISSN: 0014-3022 (Print)
eISSN: 1421-9913 (Online)

For additional information: https://www.karger.com/ENE

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