nach oben

Neurological Sciences

Erschienen in:

26.04.2022 | Original Article

Shape deformations of the basal ganglia in patients with classical trigeminal neuralgia: a cross-sectional evaluation

verfasst von: Hui Xu, Ming Zhang, Yuan Wang

Erschienen in: Neurological Sciences | Ausgabe 8/2022

Einloggen, um Zugang zu erhalten

Abstract

Introduction

Despite the involvement of subcortical brain structures in the pathogenesis of classic trigeminal neuralgia (CTN), the details of morphological abnormalities of basal ganglia to this disorder are still unknown. This study aimed to investigate potential changes in terms of volume and shape of subcortical regions in patients with CTN.

Methods

Forty-eight patients with CTN and 46 matched healthy subjects were recruited in the study. The whole-brain T1 anatomical data was acquired at a 3.0 Tesla scanner using a fast spoiled gradient recalled sequence (FSPGR). Vertex-wise analysis was applied to detect the alterations of volume and shape in each subcortical region in the patients with CTN compared to healthy controls. The relationships of morphological abnormalities in subcortical structures to the severity of orofacial pain and the affective disturbance in the patient group were examined using the multiple linear regression model.

Results

No group difference was found about volumetric measurement in any of the subcortical regions. Vertex-wise analysis revealed areas of significant shape atrophy in bilateral putamen and bilateral pallidum in the patients with CTN compared to healthy controls. Besides, the patient group exhibited shape expansion in the head of the right caudate nucleus compared to healthy subjects. In addition, shape deformation in the head of the right caudate nucleus was positively associated with VAS score in CTN.

Conclusion

The patients with CTN display shape alterations in the specific subregions of basal ganglia, which may contribute to the pathophysiology of this refractory disorder and may be useful for translational medicine.

Nur mit Berechtigung zugänglich

Cruccu G, Finnerup NB, Jensen TS, Scholz J, Sindou M, Svensson P et al (2016) Trigeminal neuralgia: New classification and diagnostic grading for practice and research. Neurology 87(2):220–228. https://doi.org/10.1212/wnl.0000000000002840CrossRefPubMedPubMedCentral

Cruccu G, Di Stefano G, Truini A (2020) Trigeminal neuralgia. N Engl J Med 383(8):754–762. https://doi.org/10.1056/NEJMra1914484CrossRefPubMed

Bendtsen L, Zakrzewska JM, Heinskou TB, Hodaie M, Leal PRL, Nurmikko T et al (2020) Advances in diagnosis, classification, pathophysiology, and management of trigeminal neuralgia. Lancet Neurol 19(9):784–796. https://doi.org/10.1016/s1474-4422(20)30233-7CrossRefPubMed

Hao Y-b, Zhang W-j, Chen M-j, Chai Y, Zhang W-h, Wei W-b (2020) Sensitivity of magnetic resonance tomographic angiography for detecting the degree of neurovascular compression in trigeminal neuralgia. Neurol Sci 41(10):2947–51. https://doi.org/10.1007/s10072-020-04419-0CrossRefPubMedPubMedCentral

Rapisarda A Baroni S Gentili V Moretti G Burattini B Sarlo F et al (2022) The role of biomarkers in drug-resistant trigeminal neuralgia: a prospective study in patients submitted to surgical treatment. Neuro Sci. https://doi.org/10.1007/s10072-022-05971-7

Kakizawa Y, Seguchi T, Kodama K, Ogiwara T, Sasaki T, Goto T et al (2008) Anatomical study of the trigeminal and facial cranial nerves with the aid of 3.0-tesla magnetic resonance imaging. J Neurosurg 108(3):483–90. https://doi.org/10.3171/jns/2008/108/3/0483CrossRefPubMed

Adamczyk M, Bulski T, Sowińska J, Furmanek A, Bekiesińska-Figatowska M (2007) Trigeminal nerve - artery contact in people without trigeminal neuralgia - MR study. Med Sci Monit Int Med J Exp Clin Res 13(Suppl 1):38–43

Ramesh VG, Premkumar G (2009) An anatomical study of the neurovascular relationships at the trigeminal root entry zone. J Clin Neurosci 16(7):934–936. https://doi.org/10.1016/j.jocn.2008.09.011CrossRefPubMed

Obermann M, Rodriguez-Raecke R, Naegel S, Holle D, Mueller D, Yoon MS et al (2013) Gray matter volume reduction reflects chronic pain in trigeminal neuralgia. Neuroimage 74:352–358. https://doi.org/10.1016/j.neuroimage.2013.02.029CrossRefPubMed

10.

Wang Y, Cao D-y, Remeniuk B, Krimmel S, Seminowicz DA, Zhang M (2017) Altered brain structure and function associated with sensory and affective components of classic trigeminal neuralgia. Pain 158(8):1561–70CrossRef

11.

Wang Y, Yang Q, Cao D, Seminowicz D, Remeniuk B, Gao L et al (2019) Correlation between nerve atrophy, brain grey matter volume and pain severity in patients with primary trigeminal neuralgia. Cephalalgia 39(4):515–525. https://doi.org/10.1177/0333102418793643CrossRefPubMed

12.

Noorani A, Hung PS, Zhang JY, Sohng K, Laperriere N, Moayedi M et al (2022) Pain relief reverses hippocampal abnormalities in trigeminal neuralgia. J Pain 23(1):141–155. https://doi.org/10.1016/j.jpain.2021.07.004CrossRefPubMed

13.

Li M, Yan J, Li S, Wang T, Zhan W, Wen H et al (2017) Reduced volume of gray matter in patients with trigeminal neuralgia. Brain Imaging Behav 11(2):486–492. https://doi.org/10.1007/s11682-016-9529-2CrossRefPubMed

14.

Tsai YH, Yuan R, Patel D, Chandrasekaran S, Weng HH, Yang JT et al (2018) Altered structure and functional connection in patients with classical trigeminal neuralgia. Hum Brain Mapp 39(2):609–621CrossRef

15.

Patenaude B, Smith SM, Kennedy DN, Jenkinson M (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 56(3):907–922. https://doi.org/10.1016/j.neuroimage.2011.02.046CrossRefPubMed

16.

Reckziegel D, Abdullah T, Wu B, Wu B, Huang L, Schnitzer TJ et al (2021) Hippocampus shape deformation: a potential diagnostic biomarker for chronic back pain in women. Pain 162(5):1457–1467. https://doi.org/10.1097/j.pain.0000000000002143CrossRefPubMed

17.

Mao CP, Bai ZL, Zhang XN, Zhang QJ, Zhang L (2016) Abnormal subcortical brain morphology in patients with knee osteoarthritis: a cross-sectional study. Front Aging Neurosci 8:3. https://doi.org/10.3389/fnagi.2016.00003CrossRefPubMedPubMedCentral

18.

Xu H Tao Y Zhu P Li D Zhang M Bai G et al (2021) Restoration of aberrant shape of caudate sub-regions associated with cognitive function improvement in mild traumatic brain injury. J Neurotrauma. https://doi.org/10.1089/neu.2021.0426

19.

Xu H, Guo C, Luo F, Sotoodeh R, Zhang M, Wang Y (2019) Subcortical brain abnormalities and clinical relevance in patients with hemifacial spasm. Front Neurol 10:1383. https://doi.org/10.3389/fneur.2019.01383CrossRefPubMed

20.

Yang Q, Xu H, Zhang M, Wang Y, Li D (2020) Volumetric and functional connectivity alterations in patients with chronic cervical spondylotic pain. Neuroradiology 62(8):995–1001. https://doi.org/10.1007/s00234-020-02413-zCrossRefPubMed

21.

Li D Xu H Yang Q Zhang M Wang Y. Cerebral white matter alterations revealed by multiple diffusion metrics in cervical spondylotic patients with pain: a TBSS study. Pain Med. 2021. https://doi.org/10.1093/pm/pnab227

22.

Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) Fsl Neuroimage 62(2):782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015CrossRefPubMed

23.

Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A et al (2002) Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17(1):479–489CrossRef

24.

Mao CP, Yang HJ (2015) Smaller amygdala volumes in patients with chronic low back pain compared with healthy control individuals. J Pain 16(12):1366–1376. https://doi.org/10.1016/j.jpain.2015.08.012CrossRefPubMed

25.

Chudler EH, Dong WK (1995) The role of the basal ganglia in nociception and pain. Pain 60(1):3–38. https://doi.org/10.1016/0304-3959(94)00172-bCrossRefPubMed

26.

Borsook D, Upadhyay J, Chudler EH, Becerra L (2010) A key role of the basal ganglia in pain and analgesia–insights gained through human functional imaging. Mol Pain 6:27. https://doi.org/10.1186/1744-8069-6-27CrossRefPubMedPubMedCentral

27.

Lim M, O’Grady C, Cane D, Goyal A, Lynch M, Beyea S et al (2020) Threat prediction from schemas as a source of bias in pain perception. J Neurosci 40(7):1538–1548. https://doi.org/10.1523/jneurosci.2104-19.2019CrossRefPubMedPubMedCentral

28.

Gustin SM, Peck CC, Wilcox SL, Nash PG, Murray GM, Henderson LA (2011) Different pain, different brain: thalamic anatomy in neuropathic and non-neuropathic chronic pain syndromes. J Neurosci 31(16):5956–5964. https://doi.org/10.1523/jneurosci.5980-10.2011CrossRefPubMedPubMedCentral

29.

Haber SN, Calzavara R (2009) The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull 78(2):69–74. https://doi.org/10.1016/j.brainresbull.2008.09.013CrossRefPubMed

30.

Starr CJ, Sawaki L, Wittenberg GF, Burdette JH, Oshiro Y, Quevedo AS et al (2011) The contribution of the putamen to sensory aspects of pain: insights from structural connectivity and brain lesions. Brain 134(Pt 7):1987–2004. https://doi.org/10.1093/brain/awr117CrossRefPubMedPubMedCentral

31.

Schwab BC, van Wezel RJ, van Gils SA (2017) Sparse pallidal connections shape synchrony in a network model of the basal ganglia. Eur J Neurosci 45(8):1000–1012CrossRef

32.

Haber SN (2014) The place of dopamine in the cortico-basal ganglia circuit. Neuroscience 282:248–257. https://doi.org/10.1016/j.neuroscience.2014.10.008CrossRefPubMed

33.

Bishop JH, Shpaner M, Kubicki A, Clements S, Watts R, Naylor MR (2018) Structural network differences in chronic muskuloskeletal pain: Beyond fractional anisotropy. Neuroimage 182:441–455. https://doi.org/10.1016/j.neuroimage.2017.12.021CrossRefPubMed

34.

Absinta M, Rocca MA, Colombo B, Falini A, Comi G, Filippi M (2012) Selective decreased grey matter volume of the pain-matrix network in cluster headache. Cephalalgia 32(2):109–115. https://doi.org/10.1177/0333102411431334CrossRefPubMed

35.

Opris I, Lebedev M, Nelson RJ (2011) Motor planning under unpredictable reward: modulations of movement vigor and primate striatum activity. Front Neurosci 5:61. https://doi.org/10.3389/fnins.2011.00061CrossRefPubMedPubMedCentral

36.

Grahn JA, Parkinson JA, Owen AM (2008) The cognitive functions of the caudate nucleus. Prog Neurobiol 86(3):141–155. https://doi.org/10.1016/j.pneurobio.2008.09.004CrossRefPubMed

37.

Postuma RB, Dagher A (2006) Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. Cereb Cortex 16(10):1508–1521. https://doi.org/10.1093/cercor/bhj088CrossRefPubMed

38.

Schmidt-Wilcke T (2008) Variations in brain volume and regional morphology associated with chronic pain. Curr Rheumatol Rep 10(6):467–474. https://doi.org/10.1007/s11926-008-0077-7CrossRefPubMed

39.

Rodgers HM Patton R Yow J Zeczycki TN Kew K Clemens S et al (2021) Morphine resistance in spinal cord injury-related neuropathic pain in rats is associated with alterations in dopamine and dopamine-related metabolomics. J Pain. https://doi.org/10.1016/j.jpain.2021.11.009

40.

Hagelberg N, Martikainen IK, Mansikka H, Hinkka S, Någren K, Hietala J et al (2002) Dopamine D2 receptor binding in the human brain is associated with the response to painful stimulation and pain modulatory capacity. Pain 99(1–2):273–279. https://doi.org/10.1016/s0304-3959(02)00121-5CrossRefPubMed

41.

Fu J, Mu G, Qiu L, Zhao J, Ou C (2020) c-Abl-p38α signaling pathway mediates dopamine neuron loss in trigeminal neuralgia. Mol Pain 16:1744806920930855. https://doi.org/10.1177/1744806920930855CrossRefPubMedPubMedCentral

42.

Burkey AR, Carstens E, Jasmin L (1999) Dopamine reuptake inhibition in the rostral agranular insular cortex produces antinociception. J Neurosci 19(10):4169–4179. https://doi.org/10.1523/jneurosci.19-10-04169.1999CrossRefPubMedPubMedCentral

43.

Admon R, Holsen LM, Aizley H, Remington A, Whitfield-Gabrieli S, Goldstein JM et al (2015) Striatal hypersensitivity during stress in remitted individuals with recurrent depression. Biol Psychiatry 78(1):67–76. https://doi.org/10.1016/j.biopsych.2014.09.019CrossRefPubMed

Titel: Shape deformations of the basal ganglia in patients with classical trigeminal neuralgia: a cross-sectional evaluation
verfasst von: Hui Xu
Ming Zhang
Yuan Wang
Publikationsdatum: 26.04.2022
Verlag: Springer International Publishing
Erschienen in: Neurological Sciences / Ausgabe 8/2022
Print ISSN: 1590-1874
Elektronische ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-022-06091-y

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Akuter Schwindel: Wann lohnt sich eine MRT?

28.04.2024 Schwindel Nachrichten

Akuter Schwindel stellt oft eine diagnostische Herausforderung dar. Wie nützlich dabei eine MRT ist, hat eine Studie aus Finnland untersucht. Immerhin einer von sechs Patienten wurde mit akutem ischämischem Schlaganfall diagnostiziert.

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Frühe Alzheimertherapie lohnt sich

25.04.2024 AAN-Jahrestagung 2024 Nachrichten

Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.

Viel Bewegung in der Parkinsonforschung

25.04.2024 Parkinson-Krankheit Nachrichten

Neue arznei- und zellbasierte Ansätze, Frühdiagnose mit Bewegungssensoren, Rückenmarkstimulation gegen Gehblockaden – in der Parkinsonforschung tut sich einiges. Auf dem Deutschen Parkinsonkongress ging es auch viel um technische Innovationen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Abstract

Introduction

Methods

Results

Conclusion

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 8/2022

Longitudinally extensive dorsal column spinal cord lesion with sensory ganglionopathy

Expansion of the mutation and phenotypic spectrum of hereditary spastic paraplegia

Autonomic dysfunction in non-critically ill COVID-19 patients during the acute phase of disease: an observational, cross-sectional study

A snapshot of emergency neurology management in the Lombardy Region, Italy

Cognitive phenotyping of post-infectious SARS-CoV-2 patients