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Language Hemispheric Dominance Analyzed with Magnetic Resonance DTI: Correlation with the Wada Test

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Language Hemispheric Dominance Analyzed with Magnetic Resonance DTI: Correlation with the Wada Test CLINICAL ARTICLE J Neurosurg 134:1703–1710, 2021 Language hemispheric dominance analyzed with magnetic resonance DTI: correlation with the Wada test Juan Delgado-Fernández, MD,1 Maria Ángeles García-Pallero, MD,2 Rafael Manzanares-Soler, MD,3 Pilar Martín-Plasencia, PhD,4 Guillermo Blasco, MD,4 Natalia Frade-Porto, MD,4 Marta Navas-García, MD,4 Paloma Pulido, PhD,4 Rafael G. Sola, PhD,5,6 and Cristina V. Torres, PhD4 1Department of Neurosurgery, University Hospital 12 de Octubre, Madrid; 2Department of Neurosurgery, Hospital Universitario Central de Asturias, Asturias; 3Department of Radiology and 4Department of Neurosurgery, University Hospital La Princesa, Madrid; 5Department of Innovation in Neurosurgery, Universidad Autonoma de Madrid; and 6Department of Neurosurgery, Hospital del Rosario, Madrid, Spain OBJECTIVE Language lateralization is a major concern in some patients with pharmacoresistant epilepsy who will face surgery; in these patients, hemispheric dominance testing is essential to avoid further complications. The Wada test is considered the gold standard examination for language localization, but is invasive and requires many human and mate- rial resources. Functional MRI and tractography with diffusion tensor imaging (DTI) have demonstrated that they could be useful for locating language in epilepsy surgery, but there is no evidence of the correlation between the Wada test and DTI MRI in language dominance. METHODS The authors performed a retrospective review of patients who underwent a Wada test before epilepsy sur- gery at their institution from 2012 to 2017. The authors retrospectively analyzed fractional anisotropy (FA), number and length of fibers, and volume of the arcuate fasciculus and uncinate fasciculus, comparing dominant and nondominant hemispheres. RESULTS Ten patients with temporal lobe epilepsy were reviewed. Statistical analysis showed that the mean FA of the arcuate fasciculus in the dominant hemisphere was higher than in the nondominant hemisphere (0.369 vs 0.329, p = 0.049). Also, the number of fibers in the arcuate fasciculus was greater in the dominant hemisphere (881.5 vs 305.4, p = 0.003). However, no differences were found in the FA of the uncinate fasciculus or number of fibers between hemi- spheres. The length of fibers of the uncinate fasciculus was longer in the dominant side (74.4 vs 50.1 mm, p = 0.05). Volume in both bundles was more prominent in the dominant hemisphere (12.12 vs 6.48 cm3, p = 0.004, in the arcuate fasciculus, and 8.41 vs 4.16 cm3, p = 0.018, in the uncinate fasciculus). Finally, these parameters were compared in pa- tients in whom the seizure focus was situated in the dominant hemisphere: FA (0.37 vs 0.30, p = 0.05), number of fibers (114.4 vs 315.6, p = 0.014), and volume (12.58 vs 5.88 cm3, p = 0.035) in the arcuate fasciculus were found to be statisti- cally significantly higher in the dominant hemispheres. Linear discriminant analysis of FA, number of fibers, and volume of the arcuate fasciculus showed a correct discrimination in 80% of patients (p = 0.024). CONCLUSIONS The analysis of the arcuate fasciculus and other tract bundles by DTI could be a useful tool for lan- guage location testing in the preoperative study of patients with refractory epilepsy. https://thejns.org/doi/abs/10.3171/2020.4.JNS20456 KEYWORDS Wada test; MRI; DTI; diffusion tensor imaging; arcuate fasciculus; uncinate fasciculus; fractional anisotropy; hemisphere dominance; epilepsy ANGUAGE is one of the most complex functions of and Wernicke areas by the arcuate fasciculus. Currently, the brain and involves different cortical areas and the dual-stream theory of language includes the dorsal white matter fascicules. Classically, the theory of stream, involved in sensorimotor features of the language, languageL based on the anatomical findings of Wernicke and the ventral stream for speech comprenhension.1 This and Geschwind described the interconnection of the Broca model also includes the uncinate fasciculus (among oth- ABBREVIATIONS CI = confidence interval; DTI = diffusion tensor imaging; FA = fractional anisotropy; fMRI = functional MRI; ROI = region of interest. SUBMITTED February 16, 2020. ACCEPTED April 22, 2020. INCLUDE WHEN CITING Published online July 24, 2020; DOI: 10.3171/2020.4.JNS20456. ©AANS 2021, except where prohibited by US copyright law J Neurosurg Volume 134 • June 2021 1703 Unauthenticated | Downloaded 10/10/21 08:13 PM UTC Delgado-Fernández et al. ers), which connects the inferior longitudinal fasciculus to ropsychological study, and intercritical and critical video the inferior frontal area and is one of the main tracts on EEG study. In cases in which epilepsy was secondary to a the ventral stream, connecting both pathways.1,2 tumor, SPECT and EEG studies were not performed. Language is a lateralized function in most humans: 95% of right-handed people show left-sided hemispheric MRI localization, while 15% of left-handed people show right- 3 MR images of patients were acquired on a 1.5-T GE sided localization. However, in some cases an atypical scanner. Diffusion-weighted imaging was obtained using language lateralization can be identified. Different studies a single-shot echo-planar imaging sequence with the fol- have demonstrated that in patients with previous lesions lowing parameters: TR 11,000 msec, FOV 280 × 280 mm, in the left hemisphere, language lateralization is influ- matrix size 128 × 128, voxel dimensions 1.1 × 1.1 × 2.9 4–7 enced. This is the case in epilepsy patients who have mm, slice thickness 3 mm, 25 noncollinear diffusion di- demonstrated a high degree of language circuit reorgani- rections, with a b-value of 1000 sec/mm2 and 1 additional 8,9 zation, mainly in intractable seizures. volume without diffusion weighting (b = 0 sec/mm2), and In this context, a precise location of the epileptogenic 8 minutes of acquisition time. T1-weighted images were focus is mandatory, as surgery should be tailored to avoid acquired using a 3D MPRAGE sequence, providing iso- 10 damaging any underlying structures. Normally, the epi- tropic voxels of 1 × 1 × 1 mm. lepsy protocol includes scalp EEG, neuropsychological evaluation, MRI, and PET or SPECT,11,12 but in other cases Wada Test it should be extended with stereoEEG and foramen ovale All patients underwent a Wada test. A diagnostic cathe- electrodes, or subdural electrodes.13 Nevertheless, some ter was introduced through the right femoral artery sheath patients without good outcomes in epilepsy surgery could to obtain a pretest angiogram and to evaluate the cerebral benefit from further imaging, such as diffusion tensor im- vasculature. Once there was no evidence of any pathologi- aging (DTI).14,15 cal or persisting fetal connections, a 6-Fr catheter was lo- DTI has demonstrated its utility in describing the mi- cated in the internal carotid artery. Then, a combination of crostructure of white matter tracts and defining fascicules 2 ml of 1% propofol (20 mg) and etomidate (10 mg) was and bundles in preoperative planning. In addition, frac- administrated. Neurological examination was performed tional anisotropy (FA), which describes the degree of an- 16 preoperatively, at the end of the first minute, and 5 minutes isotropy of a diffusion process, is a very useful tool that after the injection. The same procedure was repeated in helps us to understand the structural integrity of axons and 17,18 the contralateral side after location of the catheter in the myelin sheaths. internal carotid artery. Neurological examination assessed Moreover, there are a large number of studies that have motor and sensory function, cranial nerves, and language. recently demonstrated a correlation between DTI and Patients were asked to name some objects, to read some functional MRI (fMRI), which could help us define lan- sentences, and to recall the names of the objects. The guage lateralization through DTI, thereby avoiding inva- 8,9,19–22 Wada test was considered positive when dysnomia ap- sive tests such as the Wada test. However, the Wada peared.10,25 test still remains the gold standard test to determine lan- guage lateralization, and if we assume that DTI correlates Fiber Tracking with Wada test results, that could lead to a possible bias. Moreover, the Wada test and fMRI do not have a perfect Based on previous data, the arcuate fasciculus and un- correlation. In a meta-analysis, Dym et al.23 reviewed 442 cinate fasciculus tracts were traced bilaterally in all pa- patients, comparing fMRI with the Wada test, and showed tients’ preoperative MR images. White matter tracts of that sensitivity and specificity of fMRI for atypical lan- both fascicles were localized using BrainLAB software guage dominance were 83.5% and 88.1%, respectively. (iPlan Cranial, version 3.0), placing two regions of inter- Nevertheless, although the Wada test remains the only est (ROIs) on a coronal and axial slice for each patient. definitive method for defining language dominance, it For the arcuate fasciculus, the first ROI was placed on a is an invasive, costly, and unpleasant experience for pa- slice above the body of the corpus callosum in a group of tients.24 Therefore, the objective of our study was to com- fibers in an anteroposterior direction running lateral to the projection fibers of the corona radiate, and the second ROI pare our results from a preoperative Wada test to DTI, so 26 DTI could be used for preoperative language lateraliza- in the superior temporal gyrus. In the uncinate fascicu- tion in the future. lus, the initial ROI was placed on a coronal view on the hook of the uncinate fasciculus (a temporomesial structure located below the anterior commissure with a main direc- Methods tion in the z-axis) and the second was drawn anteriorly to We performed a retrospective study, reviewing all the genu of the corpus callosum.27 The internal capsule patients who underwent a Wada test to determine hemi- was obtained with an ROI placed in the bulb and a second spheric dominance for language between 2012 and 2017 in the motor area, which we used as a control to check in La Princesa Hospital, Madrid.
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