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DOI 10.1007/s00701-003-0165-4
Clinical Article
Surgical resection of gliomas WHO grade II and III
located in the opercular region
1
Department of Neurosurgery, Ludwig-Maximilians-University, Munich, Germany
2
Department of Physical Medicine and Rehabilitation, Ludwig-Maximilians-University, Munich, Germany
Fig. 1. Diagrams of individual tumour extensions based on axial, coronal and sagittal T1-weighted MR images, enlarged to a standard size and
transferred to a schematic brain section (see methods). An example of a MR image in sagittal and coronal view is given
Surgical resection of gliomas WHO grade II and III located in the opercular region 11
the latter medication could be continued for the rest of the surgical Table 1. Demographic data of 14 patients with tumours in the opercular
procedure [7]. An 8 year old girl with a left sided tumour as well as 2 region
patients with the tumour in the non-dominant hemisphere underwent
surgery in general anaesthesia. Variables Total
Following opening of the dura mapping of the motor and language
Age (years) 31.1 10.1 (range 8–50)
relevant areas was performed by cortical stimulation according to the
Sex (m=f) 6=8
techniques described previously [5, 18]. The interelectrode distance of
the bipolar forceps was 4 mm. Stimulation was done with rectangular Histologic grade
pulses of 0.2 ms duration and a repetition rate of 50=s at intensities of 5 II 11
to 12 mA. The stimulation was undertaken in a systematic manner every III 3
eight to ten millimetres starting from anterior to posterior. All sites were Histologic subtype
tested at least twice, marked with a sterile numbered label and photo- fibrillary 10
graphed for documentation. From the photos the positive and negative oligoastrocytic 4
stimulation points were later on transferred to the schematic brain sec-
Symptoms (duration, months) 14.8 22.7 (range 1–82)
tion, underlayed by a 5 mm square grid. After resection was completed
Epileptic seizures 13
the distance from the posterior resection line to the next positive motor
Focal neurological deficits 5
point was measured in mm. Mapping of speech and language functions
(paresis, language deficits)
was accomplished by a confrontation naming task and the Token Test.
Signs of increased intracranial pressure 3
Visual stimuli in form of line drawings of common objects were pre-
sented to the patient together with a carrier phrase (‘‘This is a . . .’’); the Tumour location
patient’s task was to read aloud the carrier phrase and to add the article right (dominant in 2 pts.) 4
and the name of the object within the stimulation period of 4 seconds. left 10
Ojemann and Ward [16] established this technique, which allows a Surgery
distinction between speech and naming errors. A speech arrest was under local anaesthesia 11
registered whenever there was no utterance, while slowing of speech under generalized anaesthesia 3
or a dysarthric disturbance was registered as speech disturbance. An GTR 7
aphasic arrest was recorded when the carrier phrase was correctly uttered STR 7
but the name of the object could not be produced, an aphasic disturbance
was defined as an aphasic misnaming (semantic paraphasia, confusion of Gross total resection GTR; subtotal resection STR.
expressions). The methods of intraoperative language and speech mon-
itoring as well as the postoperative neuropsychological testing were
standardized over the study period in order to obtain comparable data.
Tumour resection was tailored according to the results of motor and (dominant) side, in 4 patients the tumour was on the
language mapping, and was performed under microsurgical conditions right side and two of them were left handed with the
with the use of an operating microscope. If no positive areas were found
dominant hemisphere on the right side. Seizures were
over the tumour, the resection was carried out along the visible tumour
border or along the confines of a gyrus. If several positive areas were the most common initial symptoms (13=14 ¼ 92.96%),
mapped over the tumour, the resection remained subtotal or only an generalized in 8 and focal in 5 patients. Speech distur-
extensive biopsy was undertaken. bances were present preoperatively in 5 patients, but
they occurred in 3 only after seizures. Three patients
Neuropsychological testing showed contralateral muscle weakness, one patient sen-
Neuropsychological evaluation was performed in those patients with sory deficits, one patient double vision, and 3 patients
tumours located in or near language areas. The patients were tested 1 to complained of headache.
3 days preoperatively, seen 1 to 8 days postoperatively, and 8 patients
were reevaluated up to 18 months postoperatively. Neuropsychological
testing included a standard German aphasia test (Aachener Aphasie Test
[10]); this aphasia battery (AB) consists of subtests for naming, repeti- MR-anatomy and analysis
tion, receptive and written language and the Token Test. Also included in
the neuropsychological evaluation was a test of verbal learning and The precise topography of the opercular region may
memory (VM, M€ unchner Ged€achtnistest, a German research version differ considerably. According to the publications of
of the California Verbal Learning Test [2]), in which word lists have Ebeling and Steinmetz four different types for each the
to be learned. Free and cued recall as well as recognition scores were
gained as performance indices. All patients with language or motor
anterior suprasylvian and the parietal opercular topogra-
deficits received intensive speech and physiotherapy. phy can be decerned [20, 6]. This anatomy should be
considered, when studying the location of a tumour in
these regions. The superimposed extensions of the indi-
Results
vidual tumours of the present study in sagittal and cor-
onal planes are shown in Fig. 1. All tumours involved
Clinical data and preoperative
the inferior portion of the pre- and=or postcentral gyrus;
neurological deficits
8 tumours showed a more frontal extension involving the
The demographic data of the 14 patients are presented pars opercularis respectively the pars triangularis of the
in Table 1. In 10 patients the tumour was on the left frontal lobe, while 3 tumours showed a more parietal
12 A. Peraud et al.
Pat. no. Age=sex Tumour location R=L Preoperative deficits Postoperative symptoms and deficits neuropsychological results
handedness R=L neuropsychological results
Day 1–8 1–5 months 6–18 months
1. 29=m L=R 2 Grand Maux word finding difficulties word finding difficulties –
AB, VM: no deficits AB: no formal testing not tested AB, VM: no deficits
possible: severe aphasia
VM: not tested
2. 30=m L=R Jackson epilepsy right leg – one Jackson seizure under stress
AB, VM: no deficits AB: no deficits AB, VM: no deficits not tested
VM: impaired
3. 41=f R=R intermittent weakness left arm, paresis left arm, speech apraxia speech apraxia under stress
dysarthria speech apraxia
4. 32=m L=R focal epilepsy focal epilepsy, no deficits focal epilepsy, no deficits focal epilepsy, no deficits
AB, VM: no deficits not tested not tested not tested
5. 8=f L=R Jackson epilepsy, Grand mal, mild paresis of left thumb, focal epilepsy, no speech deficits focal epilepsy
speech apraxia speech apraxia
6. 36=f L=R focal and generalized seizures – – –
AB, VM: no deficits not tested AB, VM: no deficits AB, VM: no deficits
7. 41=f L=R generalized seizures with hemiparesis right side mild paresis of right arm, no sensory discrimination
postictal aphasia pronounced on arm no sensory discrimination for temperature
for temperature, speech
apraxia under stress
Surgical resection of gliomas WHO grade II and III located in the opercular region
AB, VM: no deficits AB: repetition mildly impaired, not tested AB, VM: no deficits
VM: no deficits
8. 28=m R=R Grand mal mild paresis of left hand – seizures under stress
9. 28=f L=R focal seizure, mild hemiparesis pronounced hemiparesis, residual hemiparesis arm residual hemiparesis, dysarthric speech
right side, dysarthric speech, word dysarthric speech more than leg, dysarthric under stress
finding difficulties speech
AB: repetition impaired AB: repetition, reading, not tested not tested
naming impaired: aphasia
VM: impaired VM: no deficit
10. 22=f L=R grand mal with postictal mild paresis right hand, epileptic seizure, no other deficit
aphasic disturbance speech disturbance
AB, VM: no deficits AB: repetition, naming not tested AB, VM: no deficits
impaired,
VM: no deficit
(continued)
13
14
Table 2 (continued)
Pat. no. Age=sex Tumour location R=L Preoperative deficits Postoperative symptoms and deficits neuropsychological results
handedness R=L neuropsychological results
Day 1–8 1–5 months 6–18 months
which resolved within 3 months. This syndrome consisted surgery in this region becomes extremely delicate.
of bilateral dysfunction of the face, pharynx, tongue, and Initially, we assumed, that in analogy to astrocytomas
muscles of mastication, and the patient was unable to WHO grade II in the temporal lobe or supplementary
speak [3]. The authors related these deficits to injury of motor area [17], functional important sites would be
the corticosubcortical facial motor structures, and strong- found outside the tumour, displaced during tumour
ly recommended intraoperative functional mapping and growth, and could thus be identified and spared. This
awake surgery in order to identify these pathways. was the case for instance in patients represented in
In the present study with tumours involving the opercu- Fig. 2a and b. However in approximately 50% of all
lar region, the motor cortex respectively motor relevant patients functional important sites were detected in
areas were rather constant and could be easily defined by the cortex overlying the tumour. This is in contrast to
stimulation. This is helpful for orientation. In about 50% low grade astrocytomas of the superior frontal gyrus
of the cases, motor cortex was displaced by the tumour in or the temporal lobe, where positive stimulation sites
a superior or anterior direction, while in the other 50% were found only in 4.3% and 5% of the patients over
motor function was found in the cortex overlying the the tumour, respectively [17, 18]. In addition, we
tumour. Consequently, this cortex may still bear function. initially suggested that such sites are probably no
In contrast to the motor cortex, the distribution of speech longer involved in the language network, but the def-
relevant stimulation points was extremely variable. Only icits following resection or surgical undermining of
the retrospective analysis (Fig. 3) demonstrated that areas one or several sites in 3 patients demonstrated that
at which speech was arrested or disturbed (speech apraxia) these sites still bear important language functions.
were located predominantly in the motor cortex and may With these clinical experiences we became con-
represent the above described common motor-language vinced that such areas must be protected or even that
cortex. Such areas may be responsible for the final cortical resection has to be abandoned if mapping showed
motor pathway of speech. Areas where aphasic arrest important function over the tumour. Consequently,
resulted from stimulation (the carrier phrase was uttered, only 7 out of 14 patients were amenable for complete
but naming was disturbed) were in general located more tumour removal.
anteriorly, and this corresponds more or less to the Broca c) This study supports previous reports [8, 17], and
area (Fig. 3). Due to the relative large extension of the demonstrates that a safety margin of at least 0.5 cm,
two areas, any individual prediction of functional relevant according to Haglund and coworkers even > 1 cm,
areas was impossible and the intraoperative localisation from the next positive motor or language site is
was only possible with cortical stimulation. necessary to avoid persistent functionally disabling
deficits. This simple paradigm will be of great use
Surgical conclusions for neurosurgeons who perform surgery within this or
other functional important cortical regions.
Despite the retrospective character of our study and
d) A critical discussion of the technique of cortical elec-
the possible bias in treatment strategies, our findings
trical stimulation, although presently accepted as the
may lead to some essential conclusions:
method of choice for speech mapping, seems appro-
a) This spatial separation of two cortical areas with dif- priate. Bipolar stimulation, even at low intensities,
occasionally may induce a focal seizure in the oro-
ferent language function may explain the two most
facial or hand=arm muscles of short duration. Local
important postoperative speech deficits, which are
application of cold Ringer’s lactate on the cortex was
either apraxic or aphasic in nature. The pure aphasia
recommended to rapidly terminate them [19].
syndrome is related to areas with aphasic arrest, and
Recently, Neuloh and Schramm advocated the use
this deficit recovered fast in the present cases (Broca
of monopolar stimulation to reduce this risk [13].
area) (Fig. 3). Areas with speech arrest are mainly
e) An important question is whether in the future func-
located in the motor cortex and seem to share common
tional MR may replace intraoperative cortical stimu-
brain mechanisms, e.g. motor and language function.
lation. By using neuronavigation, the preoperative
Disturbances of such areas cause the so-called speech
MR-data including localisation of specific functions
apraxia syndrome. The recovery of such deficits was
more prolonged in the cases presented here. can be superimposed to the intraoperative situation.
However, the unsolved problem of brainshift carries a
b) Since such functional important sites are densely and
non-negligible risk of mislocation. A comparison of
not predictably distributed over the opercular cortex,
Surgical resection of gliomas WHO grade II and III located in the opercular region 17
pre- and intraoperative language areas with the same 14. Ojemann GA (1982) Interrelationships in the localization of
language, memory, and motor mechanisms in human cortex and
naming task, by PET technique and cortical stimula- thalamus. In: Thompson RA et al (eds) New perspectives in cerebral
tion respectively, showed only a correlation of 84% localization. Raven Press, New York, pp 157–175
of the tested sites. The positive PET site was always 15. Ojemann GA, Mateer C (1979) Human language cortex: Localiza-
tion of memory, syntax, and sequential motor-phoneme identifica-
less delineated than the positive stimulation site [9].
tion systems. Science 205: 1401–1403
At present, these facts make clear that intraoperative 16. Ojemann GA, Ward AA (1971) Speech representation in ventro-
stimulation techniques are still most accurate and can lateral thalamus. Brain 94: 669–680
17. Peraud A, Meschede M, Eisner W, Ilmberger J, Reulen HJ (2002)
not be replaced by any other tool.
Surgical resection of grade II astrocytomas in the superior frontal
On the other side, preoperative functional MR may help gyrus. Neurosurgery 50: 966–977
18. Reulen HJ, Schmid UD, Ilmberger J, Eisner W, Bise K
to clarify the question, whether functional important (1997) Tumor surgery of the speech cortex in local anesthesia.
areas are overlying the tumour or are definitively outside Neuropsychological and neurophysiological monitoring during
the tumour volume. If this is the case, an alternative operations in the dominant hemisphere. Nervenarzt 68:
813–824
mode of treatment may be considered, and open tumour
19. Sartorius CJ, Berger MS (1998) Rapid termination of intraoperative
resection may be reserved for those cases where func- stimulation-evoked seizures with application of cold Ringer’s
tional important areas lay clearly 0.5 cm or more outside lactate to the cortex. Technical note. J Neurosurg 88: 349–351
20. Steinmetz H, Ebeling U, Huang Y, Kahn T (1990) Sulcus topo-
the tumour border.
graphy of the parietal opercular region: an anatomic and MR study.
Brain Lang 38: 515–533
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18 A. Peraud et al.: Surgical resection of gliomas WHO grade II and III located in the opercular region
functional deficits and their correlation with tumour location and extent documentation of tumour location, intraoperative stimulation and func-
of resection. The scientific approach is valid and its minor shortcomings tional consequences of stimulation and surgical resection.
are adequately discussed. The ‘Discussion’ briefly reviews the anatomy J. M. Baehring
of the opercular cortex and outlines the implications of this study’s
findings on surgical technique. Correspondence: Dr. Aurelia Peraud, Klinikum Grosshadern, Department
Although similar studies have been published in the past, the of Neurosurgery, Marchioninistrasse 15, 81377 Munich, Germany. e-mails:
article stands out due to its systematic approach and the excellent AureliaPeraud@aol.com, Aurelia.Peraud@med.uni-muenchen.de