Gliomas of the Cingulate Gyrus: Surgical Management and Functional Outcome

Neurosurg Focus 27 (2):E9, 2009

Gliomas of the cingulate gyrus: surgical management and functional outcome

Ma r e c v o n Le h e , M.D., a n d Jo h a n n e s Sc h r a mm , M.D. Neurochirurgische Klinik, Universitätsklinik Bonn, Germany

Object. In this paper, the authors’ goal was to summarize their experience with the surgical treatment of gliomas arising from the cingulate gyrus. Methods. The authors analyzed preoperative data, surgical strategies, complications, and functional outcome in a series of 34 patients (mean age 42 years, range 12–69 years; 14 females) who underwent 38 operations between May 2001 and November 2008. Results. In 7 cases (18%) the tumor was located in the posterior (parietal) part of the cingulate gyrus, and in 31 (82%) the tumor was in the anterior (frontal) part. In 10 cases (26%) the glioma was solely located in the cingulate gyrus, and in 28 cases (74%) the tumor extended to the supracingular frontal/parietal cortex. Most cases (23 [61%]) had seizures as the presenting symptom, 8 patients (24%) suffered from a hemiparesis/hemihypesthesia, and 4 patients (12%) had aphasic symptoms. The authors chose an interhemispheric approach for tumor resection in 11 (29%) and a transcortical approach in 27 (71%) cases; intraoperative electrophysiological monitoring was applied in 23 (61%) and neuronavigation in 15 (39%) cases. A > 90% resection was achieved in 32 (84%) and > 70% in another 5 (13%) cases. Tumors were classified as low-grade gliomas in 11 cases (29%). A glioblastoma multiforme (WHO Grade IV, 10 cases [26%]) and oligoastrocytoma (WHO Grade III, 9 cases [24%]) were the most frequent histopathological results. Postoperatively, patients in 13 cases suffered from a transient supplementary motor area syndrome (34%), all of whom had tumors in the anterior cingulate gyrus. In the early postoperative period (30 days) a new deficit occurred in 5 cases (13%, mild motor deficits or aphasic symptoms). One patient had a major bleeding episode 2 days after surgery and was in a persistent vegetative state. Conclusions. Gliomas arising from the cingulate gyrus are rare. A gross-total resection is often possible and acceptably safe; intraoperative monitoring and neuronavigation are helpful adjuncts. In case of resection of gliomas arising from the anterior cingulate gyrus a supplementary motor area syndrome has to be considered, particularly when the tumor extends to the supracingular cortex. (DOI: 10.3171/2009.6.FOCUS09104)

Ke y Wo r d s • cingulate gyrus • glioma • outcome

h e cingulate gyrus surrounds the corpus callosum ropsychological findings,2,21 functional and diffusion ten- in a belt-shaped manner at the mesial aspect of the sor imaging,1,10 lesion studies,3,11 and electrophysiological cerebral hemispheres. It is divided into anterior stimulation studies with implanted electrodes.5,18,22 For T(frontal lobe) and posterior (parietal lobe) portions in the an excellent review of data regarding the complex func- area of the central sulcus. The rostral part surrounds the tional role of the cingulate gyrus and the surrounding genu of the corpus callosum and ends in the subcallosal structures of the frontal lobe, see Rushworth et al.15 cortex; it continues posteriorly around the splenium of the The literature concerning surgical intervention in the corpus callosum to become the parahippocampal gyrus at cingulate gyrus mostly comprises data about functional the level of the cingulate isthmus. The adjacent areas of (stereotactic) neurosurgery for intractable pain,25 depres- the hemisphere comprise the mesial and hemispheric sur- sion,19 or compulsive disorders.14 Additionally, there are face of F1 with the SMA, the paracentral lobule, and the a few small series or case reports about focal epilepsy precuneus in the parietal lobe (we summarized the areas arising from neoplastic and other lesions of the cingu- adjacent to the cingulate gyrus at the interhemispheric late gyrus and surgical treatment for seizure control.8,12,26 surface as “supracingular”). The largest series so far for surgical management of tu- Functionally, the cingulate gyrus is part of the limbic mors arising from the cingulate gyrus was presented by system with extensive connectivity to different anatomi- Yaşargil et al. in 1996.24 A recent study summarized data cal and functional areas. In the last decade many studies in patients with intermediate gliomas (WHO Grades II were published concerning the cingulate area and neu- and III) arising from the anterior cingulate gyrus.20 Tak- en together, little is known about functional outcome af- Abbreviations used in this paper: F1 = superior frontal gyrus; ter resection in this circumscribed area. In this study we GBM = glioblastoma multiforme; GTR = gross-total resection; report on a homogeneous group of patients, examine the KPS = Karnofsky Performance Scale; SMA = supplementary motor risks of tumor removal, and balance different factors for area. postoperative deficits.

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TABLE 1: Presenting symptoms according to site and extent of the glioma and tumor grade*

No. of Patients (%) Sporadic Refractory KPS Score Seizures Epilepsy HP Aphasia <80 Site & Type Overall Total (17 cases) (6 cases) (6 cases) (4 cases) (6 cases) anterior cingulate gyrus 31 (81.6) pure 7 (22.6) 4 1 0 0 0 ext supracingular 24 (77.4) 11 4 4 3 5 posterior cingulate gyrus 7 (18.4) pure 3 (42.9) 1 1 1 ext supracingular† 4 (57.1) 1 1 1 1 tumor grade (WHO) LGG 11 (28.9) 4 6 0 1 0 HGG 27 (71.1) 13 0 6 3 6

* ext = extended; HGG = high-grade glioma (WHO Grades III and IV); HP = hemiparesis; LGG= low-grade glioma (WHO Grades I and II). † One patient had temporomesial infiltration.

Methods Radiological and Histopathological Data Patients and Clinical Data All patients underwent at least 1 MR imaging study preoperatively for evaluation of tumor location and infil- Between May 2001 and November 2008, we oper- tration in surrounding areas. The degree of resection was ated on 996 patients for supratentorial glial tumors in the measured according to postoperative CT/MR imaging in Department of Neurosurgery at the University of Bonn 26 cases and according to the surgeons’ impressions in (1072 resections total). The data of 38 consecutive opera- 12 cases. All histopathological diagnoses were made at tions (3.5% of all resections) in 34 patients harboring a the Department of Neuropathology/German Brain Tumor glioma arising from the cingulate gyrus were identified Reference Center at the University of Bonn based on the by a review of patients’ charts, surgery reports, and MR WHO criteria.6 imaging. The mean age of the included patients was 42 years (range 12–69 years); 14 (41%) were female. Right- Statistical Analysis sided resections were performed in 12 cases (32%). We excluded patients with tumors primarily arising from F1 Dichotomous discrete variables were analyzed using and reaching the roof of the lateral ventricle and the su- the chi-square test or Fisher exact test. A probability level pracingular aspect of the frontal lobe. of 0.05 was accepted for the indication of statistical sig- Preoperative and postoperative data were collected nificance in double-sided testing. Commercially available through a chart review and analyzed using a computer- software was used for statistical analysis (version 17.0, ized data bank. We included the age of the patients, pre- SPSS, Inc.). senting signs and symptoms, site of resection, postopera- Results tive deficits, local and systemic complications, pre- and postoperative KPS scores (10–100), and changes in KPS Clinical Data score after surgery until discharge or during the 30-day The common presenting symptoms were seizures (23 postoperative period. cases [61%]; Table 1). In addition to 6 cases (16%) with long-lasting refractory epilepsy, we found 17 cases (45%) Surgical Management in which the patients had a recent onset of seizures; in 1 We routinely recommended a tumor resection for sus- patient the seizures were combined with dysphasic symp- pected gliomas if a complete resection was possible or at toms. In 6 cases (16%) the patients had a hemiparesis, and least a meaningful cytoreduction seemed feasible (defined in 3 cases the patients had left-sided gliomas combined as > 70%). As in a recent study we defined tumor resections with dysphasic symptoms (overall 4 cases of patients with as > 90% (no or only minimal residual tumor), 90–70%, dysphasia [11%]). Patients in 2 cases (5%) presented with a and partial.17 Operative details comprised side and extent hemihypesthesia (tumor located in the posterior cingulate of surgery (pure cingulate resection or extending to adja- gyrus). In most patients it took a few days (up to 1 month) cent regions) and the approach to the tumor. In case of in- from the first presenting symptoms until CT/MR imag- volvement of the central area or the motor tract we routine- ing. In cases of refractory epilepsy the mean duration was ly used electrophysiological monitoring (continuous motor 12 years (range 3–28 years). The tumor was found inci- and somatosensory evoked potential recording and phase dentally in 3 patients (MR imaging for chronic earache/ reversal); in some cases neuronavigation was applied. deafness, after a minor trauma, or migraine, respectively).

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Fig. 1. Contrast-enhanced sagittal T1-weighted (A) and coronal FLAIR (B) MR images obtained preoperatively. Contrast- enhanced T1-weighted (C) and coronal FLAIR (D) MR images obtained postoperatively. These images show an oligoastrocytoma (WHO Grade III) in the left anterior cingulate gyrus with a large cyst and frontomesial and insular infiltration. This patient presented with hemiparesis and aphasia.

One patient had acute bleeding of a GBM in the anterior of the cingulate gyrus (31 cases [82%]), and in 7 cases cingulate gyrus with occlusion of the ipsilateral Monro (18%) the tumor was solely located in the anterior cingu- foramen and progressive loss of consciousness. late gyrus (Figs. 1 and 2). Three patients with gliomas in Five patients underwent previous treatment before the the rostral part of the anterior cingulate gyrus had tumor referral to our department. Three patients had stereotactic spread to the frontoorbital cortex, and in 1 patient the tu- biopsies, and in 1 case the patient underwent implantation mor reached the insular cortex (Fig. 1). of intraparenchymal seeds (WHO Grade II astrocytoma); In 3 cases (8%) the patients had a glioma solely in the 1 patient received local radiation without histopathologi- posterior cingulate gyrus (Fig. 3), and in 4 (11% of total) cal proof of diagnosis; 1 patient with temporomesial in- of the 7 cases of gliomas in the posterior cingulate gyrus filtration of a tumor arising from the posterior cingulate the tumor infiltrated supracingular structures of the pari- gyrus had undergone a temporal lobectomy (WHO Grade etal lobe; in 1 patient the tumor extended to the temporal II oligoastrocytoma). lobe with infiltration of the hippocampus and amygdala. The mean preoperative KPS score was 90 (range Overall, in 4 cases (11%) the patients had a limbic spread 60–100); 6 patients had a KPS score < 80, and all of these of tumors beyond the infiltration of the cingulate gyrus. patients had a supracingular infiltration. Preoperatively, According to MR imaging criteria, in 16 cases (42%) patients with high-grade gliomas were in significantly the glioma infiltrated the corpus callosum; in 2 of these worse condition and had more often neurological deficits cases there was an infiltration of the contralateral hemi- (p < 0.01). All patients with refractory epilepsy harbored sphere, and in 1 case the glioma reached the caput of the low-grade gliomas. caudate nucleus. Radiological Data Intraoperative Approach Most patients had a glioma arising in the anterior part We chose an interhemispheric approach for tumor

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fer a large enough craniotomy in an anterior-posterior orientation to be able to avoid bridging veins or retrac- tion of the overlying central cortex. The identification of the callosomarginal and the pericallosal arteries is often difficult because of bulging of the tumor mass that overlaps the vessels. A contralateral extension of the tumor was quite common, and in some cases even the falx or the arachnoid membrane of the contralateral mesial surface was infiltrated. Neuronavigation is helpful for planning the trepanation and the approach to the tumor. A transcortical approach is appropriate if the tumor extends to the supracingular structures and reaches the surface of the hemisphere. In most cases the margins of the tumor were apparent at the surface, and if necessary the relation to the central sulcus was identified electro- physiologically (phase reversal). The vessels of the interhemispheric cleft were preserved with debulking of the tumor and subpial resection at the mesial surface. As mentioned above, this procedure might be misleading if the tumor did not respect the arachnoid membrane. In 18 cases (47%) we opened the lateral ventricle to remove the tumor completely; in 6 cases (all tumors with extended infiltration of the frontal lobe) the surgeon left a closed drain in the wide-opened ventricle, which was to be opened in case a blood clot caused an occlusive hy- drocephalus. In all patients the drain was removed after 3 days. One of these patients suffered from a transient meningeal inflammation (aseptic meningitis) 5 days after removing the drain. A > 90% tumor resection was achieved in 32 cases Fig. 2. Axial MR images. Contrast-enhanced axial T1-weighted (A) (84%) and > 70% in another 5 cases (13%). In this lat- and FLAIR (B) MR images obtained preoperatively. Contrast-enhanced ter group of patients the tumor had infiltrated the central axial T1-weighted (C) and FLAIR (D) MR images obtained postop- area, the basal ganglia, or the contralateral corpus callo- eratively. These images show an astrocytoma (WHO Grade II) in the sum, so that a GTR was not possible. Four cases in which right anterior cingulate gyrus. The patient presented with occasional seizures. reoperation was performed were included in the series. In 1 patient the surgery was stopped at < 70% resection of the tumor due to intraoperative technical breakdown resection in 11 cases, of which 9 had no supracingular of electrophysiological monitoring. We completed the extension (90% of all pure cingulate gliomas). In 1 patient resection of the remaining tumor near the motor cortex with a tumor solely in the right dorsal cingulate gyrus after 12 weeks when the initial SMA syndrome was re- and previous stereotactic biopsy, the interhemispheric ap- solved (WHO Grade III oligoastrocytoma in the anterior proach was not possible due to adhesions and large bridg- cingulate gyrus). ing veins. In 2 patients the tumor infiltrated the medial Of the other 3 patients with repeated surgeries, 2 frontal gyrus, but it did not reach the surface of the hemi- underwent surgery for tumor recurrence (a WHO Grade sphere so that an interhemispheric approach was appro- II oligoastrocytoma transformed into a WHO Grade III priate to preserve F1. oligoastrocytoma after 84 months; an anaplastic astro- In the case of an interhemispheric approach, we pre- cytoma transformed into a WHO Grade IV GBM after

Fig. 3. Preoperative MR images. Coronal FLAIR (A), sagittal contrast-enhanced T1-weighted (B), and axial T2-weighted (C) images showing an oligoastrocytoma (WHO Grade III) in the right posterior cingulate gyrus with contralateral bulging. The patient presented with hemiparesis.

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TABLE 2: Postoperative functional deficits*

No. of Cases (%) KPS Score KPS Score SMA S HP Worse >20 <80 Location & Tumor Type Total (13 cases) (4 cases) (5 cases)† (11 cases) anterior cingulate gyrus 31 (81.6) pure 7 (22.6) 2 0 0 1 ext supracingular 24 (77.4) 11 2 3 5 posterior cingulate gyrus 7 (18.4) pure 3 (42.9) 0 1 2 3 ext supracingular‡ 4 (57.1) 0 1 0 2 tumor grade (WHO) LGG 11 (28.9) 5 0 0 2 HGG 27 (71.1) 8 4 5 9 age (yrs) <50 25 (65.8) 9 2 3 6 ≥50 13 (34.2) 4 2 2 5 extent of resection (%) ≥90 32 (83.2) 10 3 4 8 <90 6 (16.8) 3 1 1 3 preop KPS ≥80 32 (83.2) 12 4 5 10 <80 6 (16.8) 1 0 0 1

* There was no statistical correlation between location, tumor grade, age of patients, extent of resection, or KPS score, and postoperative deficits. Abbreviation: S = syndrome. † This column represents patients whose KPS scores declined > 20 points. ‡ One patient had temporomesial infiltration.

38 months), 1 patient with refractory epilepsy continued SMA syndrome and tumor size, histological entity, or ex- to have seizures and was referred for complete lesion- tent of tumor resection (pure cingulate vs cingulate with ectomy after 8 months (histopathological result: WHO supracingular infiltration). Grade I dysembryoplastic neuroepithelial tumor). In 1 After a 30-day period (or at discharge) 4 patients had patient with a GBM (WHO Grade IV) in the left anterior residual paresis of the leg; 3 of the 4 patients were able cingulate gyrus with supracingular and callosal infiltra- to walk without aid, and 1 patient had additional reduced tion, major bleeding occurred 2 days after surgery and fine motor skills of the hand. Of these patients, 2 had tu- required revision. Resection was done with the aid of in- mors in the anterior cingulate gyrus and the other 2 had traoperative electrophysiological monitoring (continuous tumors in the posterior cingulate gyrus. Both patients with motor evoked potential [MEP] recording and phase re- tumors in the anterior cingulate gyrus had supracingu- versal) in 23 cases (61%) and with neuronavigation in 15 lar extension approximate to the motor strip. In 1 patient cases (39%, in 5 cases with image-fusion of fiber tracking the initial mutism resolved to a distinct anomia at dis- [diffusion tensor imaging]). charge. The patient who needed revision after a bleeding episode 2 days postoperatively remained in a vegetative Functional Outcome state. Thus, overall permanent morbidity was 16% (that Patients in 13 cases (34%) who underwent tumor is, deficits lasting longer than the hospital stay or longer resection in the anterior cingulate gyrus suffered from than 30 days). We found no statistical correlation between different degrees and duration of transient neurological the incidence of permanent neurological deficits and loca- impairment (SMA syndrome) (Table 2). Eleven of them tion of the glioma (either anterior vs posterior cingulate had a supracingular extension (85% of all patients with gyrus or pure cingulate vs cingulate with supracingular SMA syndrome postoperatively; 46% of all patients with infiltration). tumors infiltrating the supracingular area). Nine patients In the short-term observation period, the mean post- had a motor deficit, 2 had aphasic symptoms, and 2 pa- operative KPS score was 80 (range 20–100); 11 patients tients had a combination of both. All patients with speech had a KPS score < 80 and 5 patients had a deterioration of disturbances had resections in the left hemisphere. There > 20 in score. There was no statistical correlation between was no statistical correlation between the occurrence of the postoperative KPS score or change in KPS score and

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Unauthenticated | Downloaded 09/28/21 06:51 AM UTC M. von Lehe and J. Schramm location of the glioma (either anterior vs posterior cin- TABLE 3: Histopathological results* gulate gyrus or pure cingulate vs cingulate with supra cingular infiltration). Other potentially predictive param- Type No. of Cases (%) eters for the postoperative course such as age or tumor DNET (WHO Grade I) 2 (5.3) grade showed no statistical correlation with KPS score ganglioglioma (WHO Grade I) 3 (7.9) or postoperative deficits (transient or permanent). Three patients had an improvement of the presenting symptoms astrocytoma 12 (31.6) (2 patients with aphasia and 1 with a hemiparesis), and in (WHO Grade II) 4 (10.5) 5 patients the KPS score improved. (WHO Grade III) 8 (21.1) oligoastrocytoma 11 (28.9) Histopathological Results (WHO Grade II) 2 (5.3) Detailed histopathological results are summarized (WHO Grade III) 9 (23.7) in Table 3. More than 70% of all patients harbored malignant gliomas (WHO Grades III and IV), and 29% of GBM (WHO Grade IV) 10 (26.3) all tumors were mixed gliomas. Taking into account that 38 (100) our patients were somehow selected because of our spe- cialization in epilepsy surgery with overrepresented low- * DNET = dysembryoplastic neuroepithelial tumor. grade tumors (long-term epilepsy-associated tumors9), the distribution of high- versus low-grade tumors in this of the hemisphere. With the aid of neuronavigation and small series is similar to large series of patients with pri- electrophysiological monitoring, the orientation in the re- mary brain tumors/gliomas.4 As in all patients with su- spective area and relationship to eloquent areas of these pra- or infratentorial gliomas we routinely recommended deep-seated tumors is simplified. adjuvant radio- or chemotherapy with high-grade tumors (WHO Grades III and IV). Functional Outcome More than one-third of the patients with gliomas in Discussion the anterior cingulate gyrus suffered from different degrees of transient motor deficits and/or speech distur- Gliomas arising from the cingulate gyrus are rare. bances. Of patients with transient deficits, 85% had ex- Only 3.5% of all supratentorial gliomas surgically treated tensive supracingular resections. All patients with speech in our department were located in the anterior or posterior disturbances were resected in the presumably dominant cingulate gyrus, and most of them spread to the surround- left hemisphere. The rate of permanent, but mostly mild, ing supracingular cortex. There are few reports about sur- morbidity was 16%. Unfortunately, 1 patient had a major 20 gical treatment of gliomas in the cingulate gyrus, and bleeding episode 2 days postoperatively and remained in little is known about the functional outcome in this spe- a vegetative state. cific entity of paralimbic tumors. The SMA syndrome is a well-known sequela after surgery in the superior frontal gyrus. The incidence of Clinical Data transient deficits in the literature after resections of the As in other series, the common presenting symptoms SMA was up to 89%. Although most authors have de- for tumors of the cingulate gyrus are seizures.20 This may scribed a complete recovery after up to 3 months for mo- reflect the epileptogenic disposition of this area like other tor deficits and up to 8 months for speech disturbance, in limbic and paralimbic structures, for example, the insular all studies concerning motor deficits a low rate of mild cortex17,23 or mediobasal tumors of the temporal lobe.16 but permanent morbidity in terms of disturbed coordina- With infiltration of the surrounding cortical areas there tion is reported.7,13,27 This may reflect the “normal mor- may evolve additional symptoms such as motor or speech bidity” of resections near the central area, but perhaps deficits. Patients suffering from high-grade gliomas had resection of an SMA is not always without a long-term more often neurological deficits and worse KPS scores effect, as most authors have stated. Further studies are preoperatively than those with low-grade gliomas. needed to evaluate speech impairment in detail to see if there are any subliminal permanent deficits after resec- Intraoperative Approach tions in the SMA. The rate of GTR of gliomas in the cingulate gyrus (> In our study, SMA syndrome with motor deficits was 90%) in our series was 84%; when eloquent areas were in- more frequent when resections were done in the left fron- filtrated a substantial cytoreduction (> 70%) was achieved tal lobe (not significant). This predominance cannot be in 13%. In 1 patient a 2-step resection was necessary be- found elsewhere in the literature and may be due to the cause of technical breakdown of intraoperative monitor- small number of patients in our study. ing in the first operation. There was no new somatosensory deficit after resec- For most pure cingulate gliomas, the interhemispher- tion of gliomas of the posterior cingulate gyrus, but 2 pa- ic approach is feasible, and this approach led to complete tients (1 patient with a pure cingulate tumor and 1 with tumor resection in 9 of 10 patients. We used a transcorti- supracingular infiltration) suffered from a mild paresis in cal approach for most cases with supracingular infiltra- the contralateral leg, which likely was an effect of retrac- tion, particularly when the tumor reached the surface tion after the interhemispheric approach.

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In the short-term observation period, the rate of parametric mapping analysis. J Neurol Neurosurg Psychia- postoperative deficits was higher and the KPS score was try 77:856–862, 2006 lower in the group with high-grade gliomas, but we found 12. Nobili L, Francione S, Mai R, Cardinale F, Castana L, Tassi no statistical significance for an unfavorable course post- L, et al: Surgical treatment of drug-resistant nocturnal frontal operatively with malignant gliomas. Patients with high- lobe epilepsy. Brain 130:561–573, 2007 13. Peraud A, Meschede M, Eisner W, Ilmberger J, Reulen HJ: grade gliomas had a significantly higher rate of deficits Surgical resection of grade II astrocytomas in the superior preoperatively (see above). frontal gyrus. Neurosurgery 50:966–967, 2002 14. Richter EO, Davis KD, Hamani C, Hutchison WD, Dostrovsky Conclusions JO, Lozano AM: Cingulotomy for psychiatric disease: mi- Gliomas arising from the cingulate gyrus are rare; croelectrode guidance, a callosal reference system for docu- seizures are the predominant presenting symptoms. A menting lesion location, and clinical results. Neurosurgery 54:622–630, 2004 GTR of the mostly malignant tumors is often possible and 15. Rushworth MF, Buckley MJ, Behrens TE, Walton ME, Ban- acceptably safe. In case of resection of gliomas arising nerman DM: Functional organization of the medial frontal from the anterior cingulate gyrus, an SMA syndrome has cortex. Curr Opin Neurobiol 17:220–227, 2007 to be considered. 16. Schramm J, Aliashkevich AF: Surgery for temporal me- Disclaimer diobasal tumors: experience based on a series of 235 patients. Neurosurgery 60:285–295, 2007 The authors report no conflict of interest concerning the mate- 17. Simon M, Neuloh G, von Lehe M, Meyer B, Schramm J: Insu- rials or methods used in this study or the findings specified in this lar gliomas: the case for surgical management. J Neurosurg paper. 110:685–695, 2009 Acknowledgments 18. Sperli F, Spinelli L, Pollo C, Seeck M: Contralateral smile and laughter, but no mirth, induced by electrical stimulation of the The authors thank their colleagues from the Departments of cingulate cortex. Epilepsia 47:440–443, 2006 Neuroradiology and Neuropathology, University Hospital Bonn, for 19. Steele JD, Christmas D, Eljamel MS, Matthews K: Anterior continuous and productive collaboration. cingulotomy for major depression: clinical outcome and relationship to lesion characteristics. Biol Psychiatry 63:670– References 677, 2008 1. Concha L, Gross DW, Beaulieu C: Diffusion tensor trac- 20. Steiger HJ, Goppert M, Floeth F, Turowski B, Sabel M: Fron- tography of the limbic system. 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J Clin Neurosci nu P, et al: Postoperative speech disorder after medial frontal 16:214–219, 2009 surgery: role of the supplementary motor area. Neurology 26. Zaatreh MM, Spencer DD, Thompson JL, Blumenfeld H, No- 60: 587–594, 2003 votny EJ, Mattson RH, et al: Frontal lobe tumoral epilepsy: 8. Leung H, Schindler K, Clusmann H, Bien CG, Popel A, clinical, neurophysiologic features and predictors of surgical Schramm J, et al: Mesial frontal epilepsy and ictal body turning outcome. Epilepsia 43:727–733, 2002 along the horizontal body axis. Arch Neurol 65:71–77, 2008 9. Luyken C, Blumcke I, Fimmers R, Urbach H, Elger CE, Wies- 27. Zentner J, Hufnagel A, Pechstein U, Wolf HK, Schramm J: tler OD, et al: The spectrum of long-term epilepsy-associated Functional results after resective procedures involving the tumors: long-term seizure and tumor outcome and neurosur- supplementary motor area. J Neurosurg 85:542–549, 1996 gical aspects. Epilepsia 44:822–830, 2003 10. Mohamed IS, Otsubo H, Shroff M, Donner E, Drake J, Snead OC III: Magnetoencephalography and diffusion tensor imaging in gelastic seizures secondary to a cingulate gyrus lesion. Clin Neurol Neurosurg 109:182–187, 2007 Manuscript submitted April 14, 2009. 11. Nakayama N, Okumura A, Shinoda J, Nakashima T, Iwama Accepted June 1, 2009. T: Relationship between regional cerebral metabolism and Address correspondence to: Marec von Lehe, M.D., Neuro consciousness disturbance in traumatic diffuse brain injury chirurgische Universitätsklinik, Sigmund-Freud-Str. 25, 53105 without large focal lesions: an FDG-PET study with statistical Bonn, Germany. email: [email protected].

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