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 CASE REPORT Complete recovery after surgical resection of left Wernicke's area in awake patient: a brain stimulation and functional MRI study Silvio Sarubbo  & Emmanu elle Le Bars  & Sylvie Moritz-Gasser  & Hugues Duffau Received: 25 November 2010 /Revised: 10 March 2011 /Accepted: 15 May 2011 /Published online: 27 September 2011 # Springer-V erlag 2011 Introduction The left Wer ni cke's area is a corners tone of language. Alt hough its ana tomica l bound ari es were deb ate d and renewed over the years [1,  3,  30], Wernicke's territory [2] is now defined as the posterior two thirds of the superior and middle temporal gyr us [1]. This area plays a multi- modal role in language, with involvement in phonological, semantic, and syntactic processing [4,  13,  28]. Its damage genera tes dramat ic aphasi a, with a poor recovery . Conse- que ntly , Wernicke's area has bee n conside red one of the main inoperable brain regions for many decades. Here, we report the first observ ation of surgic al resection of the lef t Wernic ke's area invaded by a WHO gr ade II glioma in a right-h anded patient, with a complet e functio nal recove ry . The mechanisms of compen sation were discu ssed on the basi s of the combined data pro vid ed by intra - operati ve electric al mappin g and postop erative functional MRI. Case report History A 38-year-old right-handed (score of 90 on the Edinburgh Inventory) woman experienced partial seizures with transient language disorders. MRI revealed a left temporal tumor. A fir st awa ke sur ger y was per for med on Ma rch 2005, wit h incomple te res ect ion due to the inv olvement of lan guage are as  by the lesion. Histological examinatio n revealed a WHO grade II glioma, with 1p-19q co-deletion. The patient had no language deficit and enjoyed a normal life. However, because of sei zure rec urr ence and gr owt h of the res idu al gli oma , 12 cycles of chemothera py (temozolomide) were administrat- ed. At the end of the chemotherapy, the tumor grew again (Fig.  1a ). Thus, a second surgery was proposed 3.5 years afte r the firs t ope rati on. The pre ope rative neurolo gic al exa minati on sho wed ver y mil d langua ge dis tur bances. Indeed, the pi cture namin g tes t (ora l denomi natio n 80 (DO80)) revealed two semantic paraphasias and one anomia (77 /80 ). The semantic and pho nolog ic al flu ency (2 min ) scored res pecti vely 30 and 31. The global language evaluation (Montreal Toulouse 86 (MT86)), for spoken and written comprehension and expression) was normal. Regard- ing verbal working memory, direct and indirect spans were 7 and 5, respectively. S. Sarubbo Division of Neurosurgery, Depart ment of Neuros ciences and Rehabil itation, Azienda Ospedaliero-Universitaria S. Anna, 203 C.so Giovecca, Ferrara, Italy E. Le Bars Depart ment of Neuror adiolog y, Hôpital Gui de Chauli ac, CHU Montpellier, 80 Av Augustin Fliche, 34295 Montpellier, France S. Moritz-Gasser :  H. Duffau (*) Depart ment of Neuros urger y, Hôpital Gui de Chauliac, CHU Montpellier, 80 Av Augustin Fliche, 34295 Montpellier, France e-mail: [email protected] S. Moritz-Gasser :  H. Duffau Instit ute for Neuroscien ce of Montpe llier , INSERM U1051, Plasticity of Central Nervous System, Human Stem Cells and Glial Tumors, Hôpital Saint Eloi, CHU Montpellier, 80 Av Augustin Fliche, 34091 Montpellier, France  Neurosurg Rev (2012) 35:287   292 DOI 10.1007/s10143-011-0351-4

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  • CASE REPORT

    Complete recovery after surgical resection of left Wernicke'sarea in awake patient: a brain stimulation and functionalMRI study

    Silvio Sarubbo & Emmanuelle Le Bars &Sylvie Moritz-Gasser & Hugues Duffau

    Received: 25 November 2010 /Revised: 10 March 2011 /Accepted: 15 May 2011 /Published online: 27 September 2011# Springer-Verlag 2011

    Introduction

    The left Wernicke's area is a cornerstone of language.Although its anatomical boundaries were debated andrenewed over the years [1, 3, 30], Wernicke's territory [2]is now defined as the posterior two thirds of the superiorand middle temporal gyrus [1]. This area plays a multi-modal role in language, with involvement in phonological,semantic, and syntactic processing [4, 13, 28]. Its damagegenerates dramatic aphasia, with a poor recovery. Conse-quently, Wernicke's area has been considered one of themain inoperable brain regions for many decades.

    Here, we report the first observation of surgical resectionof the left Wernicke's area invaded by a WHO grade IIglioma in a right-handed patient, with a complete functionalrecovery. The mechanisms of compensation were discussedon the basis of the combined data provided by intra-operative electrical mapping and postoperative functionalMRI.

    Case report

    History

    A 38-year-old right-handed (score of 90 on the EdinburghInventory) woman experienced partial seizures with transientlanguage disorders. MRI revealed a left temporal tumor. Afirst awake surgery was performed on March 2005, withincomplete resection due to the involvement of language areasby the lesion. Histological examination revealed a WHOgrade II glioma, with 1p-19q co-deletion. The patient had nolanguage deficit and enjoyed a normal life. However, becauseof seizure recurrence and growth of the residual glioma,12 cycles of chemotherapy (temozolomide) were administrat-ed. At the end of the chemotherapy, the tumor grew again(Fig. 1a). Thus, a second surgery was proposed 3.5 yearsafter the first operation. The preoperative neurologicalexamination showed very mild language disturbances.Indeed, the picture naming test (oral denomination 80(DO80)) revealed two semantic paraphasias and one anomia(77/80). The semantic and phonological fluency (2 min)scored respectively 30 and 31. The global languageevaluation (Montreal Toulouse 86 (MT86)), for spoken andwritten comprehension and expression) was normal. Regard-ing verbal working memory, direct and indirect spans were 7and 5, respectively.

    S. SarubboDivision of Neurosurgery,Department of Neurosciences and Rehabilitation,Azienda Ospedaliero-Universitaria S. Anna,203 C.so Giovecca,Ferrara, Italy

    E. Le BarsDepartment of Neuroradiology, Hpital Gui de Chauliac,CHU Montpellier,80 Av Augustin Fliche,34295 Montpellier, France

    S. Moritz-Gasser :H. Duffau (*)Department of Neurosurgery, Hpital Gui de Chauliac,CHU Montpellier,80 Av Augustin Fliche,34295 Montpellier, Francee-mail: [email protected]

    S. Moritz-Gasser :H. DuffauInstitute for Neuroscience of Montpellier, INSERM U1051,Plasticity of Central Nervous System, Human Stem Cells andGlial Tumors, Hpital Saint Eloi, CHU Montpellier,80 Av Augustin Fliche,34091 Montpellier, France

    Neurosurg Rev (2012) 35:287292DOI 10.1007/s10143-011-0351-4

  • Surgery

    A second awake surgery was performed using directcortico-subcortical electrostimulation, a method extensivelydetailed by the authors in previous reports [10, 12]. Forcortical mapping, the patient was asked to perform countingand picture naming. Stimulation of the ventral premotorcortex induced speech arrest (Fig. 1b). No functional siteswere found within the anatomical Wernicke's area, i.e.,the posterior part of the superior and middle temporal gyri,allowing its resection. The tumor removal was tailoredaccording to deep functional boundaries identified byrepeated electrostimulation (Fig. 1c). Indeed, stimulationof the left insular cortex induced articulatory disturbances.In addition, stimulation of the white matter below the insulaelicited semantic paraphasias, suggesting that the resectionwas into the contact of the inferior fronto-occipitalfasciculus (IFOF) [11]. Finally, stimulation of the subcor-tical fibers running within the posterior part of the cavityelicited phonemic paraphasias, suggesting that the resectionwas into the contact of the temporal part of the arcuatefasciculus [7] and should be interrupted.

    Postoperative neuropsychological assessment

    The postoperative neurological examination (day 5) showedan improvement of the naming, with 80/80 using the DO80.The semantic/phonological fluency (51/37) improved too.

    MT86 was normal, despite some hesitations in nonwordrepetition. Finally, the semantic association test was normal.However, due to a slight impairment of verbal workingmemory (direct/indirect span, 4/4), functional rehabilitationwas performed. Two months after the surgery, the patientreturned to her normal social and professional life. At6 months, the scores were normalized: DO80 was 80/80;semantic/phonological fluency was 55/43, respectively;MT86 was normal; and direct/indirect span was 6/5,respectively.

    Control MRI showed 13 cm3 of residual tumor, due to aposterior and deep residue involving the language pathwaysas well as the anterior perforating substance (Fig. 1d).Neuropathological examination confirmed a WHO grade IIglioma. No adjuvant treatment was administrated.

    Postoperative functional MRI

    A postoperative language functional MRI was also obtainedafter language rehabilitation. All images were acquired

    Fig. 1 a Preoperative sagittalT2-weighted MRI; b intraoper-ative photograph obtained be-fore tumor removal. The tumorboundaries, identified via ultra-sonography, are marked by lettertags (AE). The stimulation ofventral premotor cortex-elicitedspeech arrest (1); c intraopera-tive photograph after tumor re-moval. The stimulation of insulainduced articulatory disturban-ces (45), the stimulation ofposterior part of arcuate fascic-ulus induced phonemic para-phasias and it constituted theposterior limit of resection (39),the stimulation of inferiorfronto-occipital fasciculus pro-duced semantic paraphasias (27)and it constituted the infero-medial limit of resection.; dpostoperative sagittal T2-weighted MRI

    Fig. 2 3D reconstruction of activations showed by postoperativefMRI for: a naming task (p

  • Neurosurg Rev (2012) 35:287292 289

  • using a 1.5-T scan (Magnetom Avanto; Siemens, Erlangen,Germany). The scanning session included high-resolutionT1-weighted anatomic images, in plane with functionalimages and blood oxygenation level-dependent contrastfunctional images. The functional magnetic resonanceimaging (fMRI) consisted of three tasks: (1) naming task(four blocks with DO80 images' selection; 8TR=3 sduration of active block, 24 s) contrasted with rest control(6TR=3 s duration of rest block, 18 s); (2) silent readingtask with different stimuli (correct sentences, phonologicalerror sentence, semantic error sentence, syntactic errorsentence, and 8TR=3 s=24 s), each one repeated fourtimes and contrasted with rest control condition (6TR=3 s=18 s); and (3) semantic matching task (20 event-relatedstimuli, duration 3 s, each one composed of two words andspaced by rest control stimuli; duration 15 s). We usedblack screen as rest control. Statistical t maps comparingactivation task with control task were generated on a voxel-by-voxel basis from the time series using SPM 8 software(http://www.fil.ion.ucl.ac.uk/spm/software/spm5). The tthreshold was set to obtain a significance level of p