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Cuneus and Fusiform Cortices Thickness Is Reduced in Trigeminal

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Cuneus and Fusiform Cortices Thickness Is Reduced in Trigeminal Parise et al. The Journal of Headache and Pain 2014, 15:17 http://www.thejournalofheadacheandpain.com/content/15/1/17 RESEARCH ARTICLE Open Access Cuneus and fusiform cortices thickness is reduced in trigeminal neuralgia Maud Parise1,2*, Tadeu Takao Almodovar Kubo1, Thomas Martin Doring1, Gustavo Tukamoto1, Maurice Vincent1,3 and Emerson Leandro Gasparetto1 Abstract Background: Chronic pain disorders are presumed to induce changes in brain grey and white matters. Few studies have focused CNS alterations in trigeminal neuralgia (TN). Methods: The aim of this study was to explore changes in white matter microstructure in TN subjects using diffusion tensor images (DTI) with tract-based spatial statistics (TBSS); and cortical thickness changes with surface based morphometry. Twenty-four patients with classical TN (37-67 y-o) and 24 healthy controls, matched for age and sex, were included in the study. Results: Comparing patients with controls, no diffusivity abnormalities of brain white matter were detected. However, a significant reduction in cortical thickness was observed at the left cuneus and left fusiform cortex in the patients group. The thickness of the fusiform cortex correlated negatively with the carbamazepine dose (p = 0.023). Conclusions: Since the cuneus and the fusiform gyrus have been related to the multisensory integration area and cognitive processing, as well as the retrieval of shock perception conveyed by Aδ fibers, our results support the role of these areas in TN pathogenesis. Whether such changes occurs as an epiphenomenon secondary to daily stimulation or represent a structural predisposition to TN in the light of peripheral vascular compression is a matter of future studies. Keywords: Trigeminal neuralgia; MRI; Brain; Cortical thickness analysis; White matter; Diffusion tensor imaging Background cross-activation between large and small afferent fibers Classical trigeminal neuralgia (TN) is characterized by (ephaptic cross-talk) [2]. This peripheral process may in- severe paroxysms of electric, shock-like pain limited to duce secondary central changes resulting in sensitization one or more divisions of the trigeminal nerve [1]. It is of nociceptive neurons at the trigeminal nucleus and/or commonly evoked by trivial stimuli but frequently oc- higher brain structures [3,4]. curs spontaneously. Abnormal high-frequency stimulation due to chronic Although TN’s pathogenesis is not fully understood, pain could likewise induce morphological changes in noci- there is increasing evidence suggesting that it may be re- ception modulatory areas. Grey matter abnormalities have lated to chronic vascular compression of the trigeminal been observed in several chronic painful conditions like nerve root entry zone (REZ). This chronic compression phantom pain, chronic back pain, fibromyalgia and chronic may lead to focal demyelination, consequent generation of head pain [5-7]. On the other hand, white matter dif- aberrant activities (ectopic discharges) and pathological fusional changes were reported in brain areas involved in sensory, modulatory and cognitive functions in tem- * Correspondence: [email protected] poromandibular disorder (TMD), cluster headache, mi- 1Department of Radiology, Clementino Fraga Filho University Hospital, Universidade Federal do Rio de Janeiro, Rua Rodolpho Paulo Rocco, 255, graine, complex regional pain syndrome CRPS and Cidade Universitária, Rio de Janeiro, CEP:21941-913, Brazil fibromyalgia [8-12]. 2Department of Surgical Specialties, Division of Neurosurgery Pedro Ernesto Two previous publications reported on reduction of University Hospital, Universidade do Estado do Rio de Janeiro, Boulevard Vinte e Oito de Setembro, 77 Vila Isabel, Rio de Janeiro, RJ CEP: 20551-900, grey matter volume (GMV) in TN using voxel-based Brazil morphometry (VBM) in brain areas related to pain Full list of author information is available at the end of the article © 2014 Parise et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Parise et al. The Journal of Headache and Pain 2014, 15:17 Page 2 of 9 http://www.thejournalofheadacheandpain.com/content/15/1/17 processing and integration [13,14]. The question remains values were determined by the method of limits, i.e. the as whether these results reflect plastic changes of the brain average from five or more successive observations. as a consequence of chronic nociceptive input or a causal factor for the development of TN. Imaging parameters The aim of this study was to investigate grey (GM) and All subjects underwent scanning in a 1.5 T MRI system white matter (WM) structural changes in TN and verify (Avanto, Siemens Medical System, Erlangen, Germany) fit- whether such changes would relate to disease duration, ted with an 8-channel phased-array head coil, the follo- medication or sensory deficits. A MRI surface-based ana- wing sequences of the brain obtained: 1) T1-weight 3D lysis was performed to approach GM abnormalities. For high-resolution magnetization-prepared rapid acquisitions assessment of WM architectural diffusion tensor imaging with gradient echoes (3D-MPRAGE) sequence (128 slices; (DTI) with factional anisotropy (FA) measurements and 1×1×1.3mm3 voxels; 256 × 256 matrix size; field of tract-based-spatial-statistics (TBSS) were used. view = 256 mm; echo time = 3.39 ms; repetition time = 2.530 ms; flip angle 7°; 1.3 mm thick slices). 2) Echo- Methods planar diffusion-weighted images, with bipolar diffusion Subjects gradients in 30 orthogonal directions (122 × 122 matrix Twenty-four consecutive patients with classical TN (18 size, field of view = 256, repetition time = 10.1 s , echo- women, 6 men) according to the International Classifica- time = 94 ms, slices = 73, slice thickness = 2 mm, interslice tion of Headache Disorders version III criteria [1] were gap = 0). To optimize the measurement of diffusion in the prospectively evaluated between May 2009 and May 2012 brain, only two b values were used (b0 = 0; b1 = 900 s/mm2). at Pedro Ernesto University Hospital. The mean age was To minimize motion artifacts the head of the subjects 55.8 ± 8.5 years. Patients with symptomatic TN, other were fixed in the head coil. All images were investigated headache disorders, chronic pain elsewhere, diabetes mel- to be free of motion or ghosting. litus, claustrophobia, psychiatric conditions, or previous TN operations were excluded. TN was located within the maxillary and/or mandibular branch of trigeminal nerve DTI analysis (V2-V3) in all but one patient, in which ophthalmic For voxelwise diffusion modeling, diffusion data were branch was also involved. TN affected the left and right analyzed using FMRIB’s Diffusion Toolbox within FSL sides in respectively 13 and 11 patients. The disease dur- 4.1 (http://www.fmrib.ox.ac.uk/fsl) [15]. After perfor- ation ranged from 1 to 17 years. Due to ethical reasons ming eddy current correction and brain extraction, FA and to prevent head movements during scans, TN pre- images for all subjects were created by fitting a tensor ventive medications were not discontinued. model to the raw diffusion data. Voxelwise statistical Twenty-four matched healthy controls (12 women, 6 analysis of the FA data was carried out using TBSS men, mean age 56.3 ± 7.8 years) were also included. (Tract-Based Spatial Statistics) [16], part of FSL. All sub- Clinical neurological examination was unremarkable in jects’ FA data were aligned into a common space using the control group. This study was conducted in accor- the nonlinear registration tool FNIRT, which uses a dance with the Declaration of Helsinki and was ap- b-spline representation of the registration warp field [17]. proved by the ethical committee of Clementino Fraga The FMRIB58_FA standard-space template was used as Filho University Hospital (Study 062/09). All patients the target in TBSS (http://www.fmrib.ox.ac.uk/fsl/data/ and controls gave written informed consent for the par- FMRIB58_FA.html). Next, the mean FA image was cre- ticipation in the study. ated and thinned to create a mean FA skeleton, which rep- resents the centers of all tracts common to the group. Measurement of tactile and pain perception thresholds Each subject’s aligned FA data were then projected onto Sensory and pain perception thresholds were obtained by this skeleton, and the resulting data were fed into voxel- using bipolar electrical stimulation with surface electrodes wise cross-subject statistics for all voxels with FA ≥ 0.30 placed on the forehead above the eyebrow (V1); on the to exclude peripheral tracts with significant inter-subject cheek (V2) and on the chin (V3) just lateral to the mental variability. The voxelwise analysis was performed using foramen. Constant-current square-wave electrical stimuli permutation-based inference (5000 permutations) correc- were delivered at a 3 Hz stimulation rate with 200 ms ted for multiple comparisons, with a threshold-free cluster pulse duration and varying intensity (Medelec stimulator - enhancement (TFCE) and significance level of p < 0.05. Vickers Medical- UK). The patient was asked to state Corrected TFCE p-value images were computed to enable when stimuli of increasing current intensity became no- the identification of differences in the FA areas between ticeable (detection threshold) and “definitely” painful (pain
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