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• Clinical Article •
Changes of cortical thickness in Parkinson's disease patients with pain: A structural MRI study
ZOU Nan  WANG Erlei  ZHANG Jinru  JI Lirong  YA Yang  BAO Yiqing  LUO Yajun  FAN Guohua 

Cite this article as ZOU N, WANG E L, ZHANG J R, et al. Changes of cortical thickness in Parkinson's disease patients with pain: A structural MRI study[J]. Chin J Magn Reson Imaging, 2024, 15(5): 13-18, 23. DOI:10.12015/issn.1674-8034.2024.05.003.


[Abstract] Objective To explore the alterations of cortical thickness (CT) in Parkinson's disease (PD) patients with pain using high-resolution structural MRI and their correlations with pain scores, revealing the neuroanatomical basis of pain in PD patients.Materials and Methods From September 2020 to March 2022, 82 PD patients diagnosed by the Neurology Department of the Second Affiliated Hospital of Soochow University and 29 pain-free normal controls (NC) from local communities were recruited. Demographic and clinical data as well as structural and MRI images of all subjects were collected. The non-motor symptoms questionnaire and the visual analog scale (VAS) were applied to pain screening and pain severity assessment. The PD patients were divided into 41 PD patients with pain (PDP) and 41 PD patients without pain (nPDP) according to the VAS scores. CT analysis steps are as follows: Frist, the structural MRI data were pre-processed by the computational anatomy toolbox 12 (CAT12) software package to get the CT maps of all subjects. Then, one-way ANOVA and post hoc analysis were used to compare the three groups. The statistical results were corrected for multiple comparisons using the threshold-free cluster enhancement (TFCE) and false discovery rate (FDR), and the threshold was set at P<0.05. Finally, the CT values of significant regions in PDP groups were extracted and partial correlated with VAS scores.Results The CT values of the right superior frontal gyrus, right middle frontal gyrus, and right pars triangularis showed significant differences among the three groups. Post hoc analysis showed that the CT values of the right middle frontal gyrus and right pars triangularis were significantly reduced in the PDP group relative to the nPDP group (P=0.033, 0.007). Compared with the NC group, the PDP group showed decreased CT in the right superior frontal gyrus, right middle frontal gyrus, and pars triangularis. There was no significant correlation between CT values of significant regions and VAS scores in PDP group (P=0.088).Conclusions The decreased CT of the prefrontal region (middle frontal gyrus and inferior frontal gyrus) may be the underlying structural basis of pain in PD patients, which might be involved in the pain through the mechanisms of pain perception and regulation, emotional processing, and cognitive processing.
[Keywords] Parkinson's disease；pain；structural magnetic resonance imaging；magnetic resonance imaging；cortical thickness；neuroanatomical

ZOU Nan1   WANG Erlei1   ZHANG Jinru2   JI Lirong2   YA Yang1   BAO Yiqing2   LUO Yajun2   FAN Guohua1*  

1 Department of Radiology, the Second Affiliated Hospital of Soochow University, Suzhou 215004, China

2 Department of Neurology and Clinical Research Center of Neurological Disease, the Second Affiliated Hospital of Soochow University, Suzhou 215004, China

Corresponding author: FAN G H, E-mail: fangh22@sina.com

Conflicts of interest   None.

Received  2023-11-14
Accepted  2024-04-30
DOI: 10.12015/issn.1674-8034.2024.05.003
Cite this article as ZOU N, WANG E L, ZHANG J R, et al. Changes of cortical thickness in Parkinson's disease patients with pain: A structural MRI study[J]. Chin J Magn Reson Imaging, 2024, 15(5): 13-18, 23. DOI:10.12015/issn.1674-8034.2024.05.003.

[1]
TOLOSA E, GARRIDO A, SCHOLZ S W, et al. Challenges in the diagnosis of Parkinson's disease[J]. Lancet Neurol, 2021, 20(5): 385-397. DOI: 10.1016/S1474-4422(21)00030-2.
[2]
CABREIRA V, MASSANO J. Parkinson's disease: Clinical review and update[J]. Acta Med Port, 2019, 32(10): 661-670. DOI: 10.20344/amp.11978.
[3]
BUHMANN C, WROBEI N, GRASHORN W, et al. Pain in Parkinson disease: a cross-sectional survey of its prevalence, specifics, and therapy[J]. J Neurol, 2017, 264(4): 758-769. DOI: 10.1007/s00415-017-8426-y.
[4]
MARQUES A, BREFEI-COURBON C. Chronic pain in Parkinson's disease: Clinical and pathophysiological aspects[J]. Rev Neurol (Paris), 2021, 177(4): 394-399. DOI: 10.1016/j.neurol.2020.06.015.
[5]
VISEUX F J F, DELVAL A, SIMONEAU M, et al. Pain and Parkinson's disease: Current mechanism and management updates[J]. Eur J Pain, 2023, 27(5): 553-567. DOI: 10.1002/ejp.2096.
[6]
FORD B. Pain in Parkinson's disease[J]. Mov Disord, 2010, 25(1): S98-S103. DOI: 10.1002/mds.22716.
[7]
ADEWUSI J K, HADJIVASSILIOU M, VINARGE-ARAGÓN A, et al. Peripheral neuropathic pain in idiopathic Parkinson's disease: Prevalence and impact on quality of life; a case controlled study[J]. J Neurol Sci, 2018, 392(10): 3-7. DOI: 10.1016/j.jns.2018.06.022.
[8]
MYLIUS V, MÖLLER J C, BOHLHALTER S, et al. Diagnosis and management of pain in Parkinson's disease: A new approach[J]. Drugs Aging, 2021, 38(7): 559-577. DOI: 10.1007/s40266-021-00867-1.
[9]
MARTINEZ-MARTIN P, MANUEL ROJO-ABUIN J, RIZOS A, et al. Distribution and impact on quality of life of the pain modalities assessed by the King's Parkinson's disease pain scale[J/OL]. NPJ Parkinson's Dis, 2017, 3: 8 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/28649608/. DOI: 10.1038/s41531-017-0009-1.
[10]
MAO C J, CHEN J P, ZHANG X Y, et al. Parkinson's disease patients with pain suffer from more severe non-motor symptoms[J]. Neurol Sci, 2015, 36(2): 263-268. DOI: 10.1007/s10072-014-1942-y.
[11]
BLANCHET P J, BREFEL-COURBON C. Chronic pain and pain processing in Parkinson's disease[J]. Prog Neuropsychopharmacology Biol Psychiatry, 2018, 87(Pt B): 200-206. DOI: 10.1016/j.pnpbp.2017.10.010.
[12]
TSENG M T, LIN C H. Pain in early-stage Parkinson's disease: Implications from clinical features to pathophysiology mechanisms[J]. J Formos Med Assoc, 2017, 116(8): 571-581. DOI: 10.1016/j.jfma.2017.04.024.
[13]
DEMIRCI N, HOLLAND M A. Cortical thickness systematically varies with curvature and depth in healthy human brains[J]. Hum Brain Mapp, 2022, 43(6): 2064-2084. DOI: 10.1002/hbm.25776.
[14]
WOODWORTH D C, HOLLY L T, MAYER E A, et al. Alterations in cortical thickness and subcortical volume are associated with neurological symptoms and neck pain in patients with cervical spondylosis[J]. Neurosurgery, 2019, 84(3): 588-598. DOI: 10.1093/neuros/nyy066.
[15]
YANG Q, WANG Z, YANG L, et al. Cortical thickness and functional connectivity abnormality in chronic headache and low back pain patients[J]. Hum Brain Mapp, 2017, 38(4): 1815-1832. DOI: 10.1002/hbm.23484.
[16]
MAGON S, SPRENGER T, OTTI A, et al. Cortical thickness alterations in chronic pain disorder: An exploratory MRI study[J]. Psychosom Med, 2018, 80(7): 592-598. DOI: 10.1097/PSY.0000000000000605.
[17]
AMIN F M, DE ICCO R, Al-KARAGHOLI MA-M, et al. Investigation of cortical thickness and volume during spontaneous attacks of migraine without aura: a 3-Tesla MRI study[J/OL]. J Headache Pain, 2021, 22(1): 98 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/34418951/. DOI: 10.1186/s10194-021-01312-9.
[18]
CHAUDHARY S, KUMARAN S S, GOYAL V, et al. Cortical thickness and gyrification index measuring cognition in Parkinson's disease[J]. Int J Neurosci, 2021, 131(10): 984-993. DOI: 10.1080/00207454.2020.1766459.
[19]
WANG E, JIA Y, YA Y, et al. Patterns of Sulcal depth and cortical thickness in Parkinson's disease[J]. Brain Imaging and Behav, 2021, 15(5): 2340-2346. DOI: 10.1007/s11682-020-00428-x.
[20]
ZANIGNI S, SAMBATI L, EVANGELISTI S, et al. Precuneal thickness and depression in Parkinson disease[J/OL]. Neurodegener Dis, 2017, 17(2-3): 97-102 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/27883992/. DOI: 10.1159/000450614.
[21]
PLETCHER C, DABBS K, BARZGARI A, et al. Cerebral cortical thickness and cognitive decline in Parkinson's disease[J/OL]. Cereb Cortex Commun, 2023, 4(1): tgac044 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/36660417/. DOI: 10.1093/texcom/tgac044.
[22]
POLLI A, WEIS L, BIUNDO R, et al. Anatomical and functional correlates of persistent pain in Parkinson's disease[J]. Mov Disord, 2016, 31(12): 1854-1864. DOI: 10.1002/mds.26826.
[23]
SHEN Y, WANG J, PENG J, et al. Abnormal connectivity model of raphe nuclei with sensory-associated cortex in Parkinson's disease with chronic pain[J]. Neurol Sci, 2022, 43(5): 3175-3185. DOI: 10.1007/s10072-022-05864-9.
[24]
COHEN S P, VASE L, HOOTEN W M. Chronic pain: an update on burden, best practices, and new advances[J]. Lancet, 2021, 397(10289): 2082-2097. DOI: 10.1016/S0140-6736(21)00393-7.
[25]
SEIGER R, GANGER S, KRANZ G S, et al. Cortical thickness estimations of freeSurfer and the CAT12 toolbox in patients with Alzheimer's disease and healthy controls[J]. J Neuroimaging, 2018, 28(5): 515-523. DOI: 10.1111/jon.12521.
[26]
WILLIAMS A C D, CRAIGG K D. Updating the definition of pain[J]. Pain, 2016, 157(11): 2420-2423. DOI: 10.1097/j.pain.0000000000000613.
[27]
YANG S, CHANG M C. Chronic pain: Structural and functional changes in brain structures and associated negative affective states[J/OL]. Int J Mol Sci, 2019, 20(13): 3130 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/31248061/. DOI: 10.3390/ijms20133130.
[28]
MERCER LINDSAY N, CHEN C, GILAM G, et al. Brain circuits for pain and its treatment[J/OL]. Sci Transl Med, 2021, 13(619): eabj7360 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/34757810/. DOI: 10.1016/j.mcna.2019.11.003.
[29]
HUANG T, LIN S H, MALEWICZ N M, et al. Identifying the pathways required for coping behaviours associated with sustained pain[J]. Nature, 2019, 565(7737): 86-90. DOI: 10.1038/s41586-018-0793-8.
[30]
DE RIDDER D, ADHIA D, VANNESTE S. The anatomy of pain and suffering in the brain and its clinical implications[J]. Neurosc Biobehav Rev, 2021, 130: 125-146. DOI: 10.1016/j.neubiorev.2021.08.013.
[31]
GANDOLFI M, GEROIN C, ANTONINI A, et al. Understanding and treating pain syndromes in Parkinson's disease[J]. Int Rev Neurobiol, 2017, 134: 827-858. DOI: 10.1016/bs.irn.2017.05.013.
[32]
BRAAK H, DEL TREDICI K, RUB U, et al. Staging of brain pathology related to sporadic Parkinson's disease[J]. Neurobiol Aging, 2003, 24(2): 197-211. DOI: 10.1016/s0197-4580(02)00065-9.
[33]
HE H, LIANG L, TANG T, et al. Progressive brain changes in Parkinson's disease: A meta-analysis of structural magnetic resonance imaging studies[J/OL]. Brain Res, 2020, 1740(10): 146847 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/32330518/. DOI: 10.1016/j.brainres.2020.146847.
[34]
MA X, SU W, LI S, et al. Cerebellar atrophy in different subtypes of Parkinson's disease[J]. J Neurol Sci, 2018, 392: 105-112. DOI: 10.1016/j.jns.2018.06.027.
[35]
WILSON H, NICCOLINI F, PELLICANO C, et al. Cortical thinning across Parkinson's disease stages and clinical correlates[J]. J Neurol Sci, 2019, 398: 31-38. DOI: 10.1016/j.jns.2019.01.020.
[36]
GAO Y, NIE K, HUANG B, et al. Changes of brain structure in Parkinson's disease patients with mild cognitive impairment analyzed via VBM technology[J]. Neurosci Lett, 2017, 658(3): 121-132. DOI: 10.1016/j.neulet.2017.08.028.
[37]
SHIN N Y, BANG M, YOO S W, et al. Cortical thickness from MRI to predict conversion from mild cognitive impairment to dementia in Parkinson disease: A machine learning-based model[J]. Radiology, 2021, 300(2): 390-399. DOI: 10.1148/radiol.2021203383.
[38]
QI X, CUI K, ZHANG Y, et al. A nociceptive neuronal ensemble in the dorsomedial prefrontal cortex underlies pain chronicity[J/OL]. Cell Rep, 2022, 41(11): 111833 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/36516746/. DOI: 10.1016/j.celrep.2022.111833.
[39]
TRACEY I. Neuroimaging of pain mechanisms[J]. Curr Opin Supportive Palliat Care, 2007, 1(2): 109-116. DOI: 10.1038/s41593-023-01455-9.
[40]
STEGEMANN A, LIU S, RETANA ROMERO O A, et al. Prefrontal engrams of long-term fear memory perpetuate pain perception[J]. Nat Neurosci, 2023, 26(5): 820-829. DOI: 10.1038/s41593-023-01291-x.
[41]
MIYASHIRO S, YAMADA Y, NAGAOKA M, et al. Pain relief associated with decreased oxyhemoglobin level in left dorsolateral prefrontal cortex[J/OL]. PloS One, 2021, 16(8): e0256626 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/34424921/. DOI: 10.1371/journal.pone.0256626.
[42]
SERAFINI R A, PRYCE K D, Zachariou V. The mesolimbic dopamine system in chronic pain and associated affective comorbidities[J]. Biol Psychiatry, 2020, 87(1): 64-73. DOI: 10.1016/j.biopsych.2019.10.018.
[43]
MILOSEVIC L, GRAMER R, KIM T H, et al. Modulation of inhibitory plasticity in basal ganglia output nuclei of patients with Parkinson's disease[J]. Neurobiol Dis, 2019, 124: 46-56. DOI: 10.1016/j.nbd.2018.10.020.
[44]
ONG W Y, STOHLER C S, HERR D R. Role of the prefrontal cortex in pain processing[J]. Mol Neurobiol, 2019, 56(2): 1137-1166. DOI: 10.1007/s12035-018-1130-9.
[45]
FORKAMNN K, GRASHORNN W, SCHMIDT K, et al. Altered neural responses to heat pain in drug-naive patients with Parkinson disease[J]. Pain, 2017, 158(8): 1408-1416. DOI: 10.1097/j.pain.0000000000000923.
[46]
SHEN Y, WANG J, PENG J, et al. Abnormal connectivity model of raphe nuclei with sensory-associated cortex in Parkinson's disease with chronic pain[J]. Neurol Sci, 2022, 43(5): 3175-3185. DOI: 10.1007/s10072-022-05864-9.
[47]
ZHOU C, GAO T, GUO T, et al. Structural covariance network disruption and functional compensation in Parkinson's disease[J/OL]. Front Aging Neurosci, 2020, 12: 199 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/32714179/. DOI: 10.3389/fnagi.2020.00199.
[48]
JIANG J, DU W, CUI Y N, et al. Brain gray matter volume and functional brain network in patients with lower back pain: a MRI study[J]. Chin J Magn Reson Imaging, 2021, 12(9): 45-48, 60. DOI: 10.12015/issn.1674-8034.2021.09.010.
[49]
MCILWRATH S L, STARR M E, HIGH A E, et al. Effect of acetyl-L-carnitine on hypersensitivity in acute recurrent caerulein-induced pancreatitis and microglial activation along the brain's pain circuitry[J]. World J Gastroenterol, 2021, 27(9): 794-814. DOI: 10.3748/wjg.v27.i9.794.
[50]
SEBBA A. Pain: A review of interleukin-6 and its roles in the pain of rheumatoid arthritis[J]. Open Access Rheumatol, 2021, 13: 31-43. DOI: 10.2147/OARRR.S291388.
[51]
MAGON S, MAY A, STANKEWITZ A, et al. Cortical abnormalities in episodic migraine: A multi-center 3T MRI study[J]. Cephalalgia, 2019, 39(5): 665-673. DOI: 10.1177/0333102418795163.
[52]
SHEN Y T, YUAN Y S, WANG M, et al. Dysfunction in superior frontal gyrus associated with diphasic dyskinesia in Parkinson's disease[J/OL]. NPJ Parkinson's Dis, 2020, 6: 30 [2023-11-14]. https://pubmed.ncbi.nlm.nih.gov/33145398/. DOI: 10.1038/s41531-020-00133-y.
[53]
TICHELAAR J G, SAYALI C, HELMICH R C, et al. Impulse control disorder in Parkinson's disease is associated with abnormal frontal value signalling[J]. Brain, 2023, 146(9): 3676-3689. DOI: 10.1093/brain/awad162.
[54]
URIBE C, SEGURA B, BAGGIO H C, et al. Cortical atrophy patterns in early Parkinson's disease patients using hierarchical cluster analysis[J]. Parkinsonism Relat Disord, 2018, 50: 3-9. DOI: 10.1016/j.parkreldis.2018.02.006.

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