Neuronavigation and epilepsy surgery

doi:10.4236/health.2010.27114

Paper Menu >>

Journal Menu >>

Vol.2, No.7, 753-758 (2010)

doi:10.4236/health.2010.27114

Health

Neuronavigation and epilepsy surgery

Martin B. Glaser1*, Konrad J. Werhahn2, Peter Grunert1, Clemens Sommer3,

Wibke Müller-Forell4, Joachim Oertel1

1Department of Neurosurgery, Unive rsity Hospital Medical Cente r, Johannes Gutenberg University, Mainz, Germany;

*Corresponding Aut hor: glaserm@uni-mainz.de

2Department of N e urology, University Hospital Medical Center, Johannes Gutenberg University, Mainz, Germany

3Department of Neuro p a th o l o gy, University Hospital Medical Center, Johannes Gutenberg University, Mainz, Germany

4Institution of Neuroradiology, University Hospital Medical Center, Johannes Gutenberg University, Mainz, Germany

Received 16 February 2010; revised 11 March 2010; accepted 12 March 2010.

ABSTRACT

Resective epilepsy surgery is an elective ther-

apy indicated in focal epilepsy patients who are

resistant to pharmacotherapy. Every effort sho-

uld be undertaken to perform the procedures as

safe and less traumatic as possible. Neurona-

vigation could represent a suitable tool to re-

duce surgical morbidity and increase surgical

radicality. Here, we present a series of 41 pa-

tients who were operated on for medically in-

tractable epilepsy using neuronavigation. Over-

all, complication rate was 17% with a favourable

seizure outcome of 88% (Engel’s class I/II). Our

data suggest that neuronavigation is a valuable

surgical technique to accomplish a favourable

outcome in epilepsy surgery.

Keywords: Neuronavigation; Epilepsy Surgery;

Outcome

1. INTRODUCTION

Epilepsy is a frequent condition. Approximately 40 mil-

lion people are affected worldwide and the prevalence of

epilepsy has been estimated to be around 0.7% [1]. The

mean annual incidence of first unprovoked seizures in

population-based studies is 56.8 per 100 000 person-

years, 23.5 per 100 000 person-years for single unpro-

voked seizures, and 33.3 per 100 000 person-years for

epilepsy (recurrent unprovoked seizures). Partial sei-

zures occur in 40-60%, two-thirds of which are temporal

lobe epilepsies [2,3]. Clinically, focal epilepsy may first

be suspected with a first witnessed report of a general-

ized tonic-clonic seizure but often seizures may be more

subtle consisting of a transient short lasting loss of con-

sciousness with or without oral or manual automatisms

or focal tonic or clonic movements affecting parts of the

body. Seizures may lead to developmental retardation,

social impairment (e.g. limited choice of profession,

ability to obtain a driving licence) and even sudden un-

expected death in epilepsy [4]. In most cases, conserva-

tive treatment with antiepileptic drugs is successful in

preventing clinical seizures, but up to 33% of patients

will prove to be resistant to medical treatment [5].

Patients with focal epilepsy are generally surgical

candidates, if medical treatment with at least two differ-

ent anticonvulsive drugs in sufficient doses fails and

disabling seizures persist. Bad prognostic factors for

medical treatment in focal epilepsy are a structural lesion

on Magnetic Resonance Imaging (MRI), particularly

with dual pathology, post-stroke scars and vascular mal-

formations having the best and cortical dysgenesis and

hippocampal sclerosis the poorest outcome [3]. Optimal

surgical results are obtained in patients with a circum-

scribed seizure onset (especially temporal/temporome-

sial) in video-EEG recordings, concordant focal pathol-

ogy on MRI (e.g. hippocampal sclerosis) and concordant

neuropsychological findings [6,7].

The need for a device enabling precise introduction of

instruments into deep intracerebral structures was first

addressed by Zernov et al. [8] 1890. He constructed a

frame which was fixed on the skull by screws. The posi-

tion of deep structures were measured from external

anatomical landmarks. Clark developed 1908 a frame

which served as a stable coordinate system for calcula-

tion of intracranial targets in relation to the frame [9,10].

In the second half of the last century these frames were

refined. More and more indications were found along

with the progress of the imaging modalities (x-ray, an-

giogram, computed tomography, MRI). Frame based

stereotactic systems are still the most accurate naviga-

tional tools and very small targets like the subthalamic

nucleus can be implanted with depth electrodes for the

treatment of parkinsonism.

M. B. Glaser et al. / HEALTH 2 (2010) 753-758

754

One major disadvantage of the stereotactic frame is

the restricted surgical field as long as the arc is in place.

At the end of the 1980s the “frameless” navigation was

developed, with first clinical applications in neurosur-

gery at the beginning of th e 1990s [11].

Nowadays, frameless neuronavigation is an accepted

tool in contemporary microneurosurgery [12-15]. Its

application contributes to make surgical approaches

smaller and less invasive [16]. Consequently neuronavi-

gation was integrated also in epilepsy surgery [17].

The neuronavigation is basically a miniature of a GPS

(general positioning system). The neuronavigation sys-

tems are able to determine the position of the tip of a

pointer in 3-D-space and to transfer the position into the

appropriate CT or MRI data set in real time during the

entire operation (in case of a microscope the focus cor-

responds to the tip of the pointer). From the technical

point of view we can distinguish between armbased and

armless navigation. The latter have the advantage not to

restrict the operative field. Different armless systems

were realized using sonic, infrared, magnetic waves or

visible light (see Figure 1). The transfer of the pointer

tip in the appropriate images makes a registration before

application necessary. Per point registration and surface

registration were developed for this purpose. The navi-

gation devices have higher flexibility but less accuracy

in comparison to the frame based systems. Regarding

navigation accuracy we have clearly to distinguish be-

tween technical accuracy of the navigation system (how

accurately the system determines the position in the 3-D-

space), registration accuracy (how accurately is the data

transfer from 3-D-space into the CT and MRI image

space) and application accuracy depending of the intra-

operative situation including brain shift [18].

Figure 1. Drawing of an armless neuronavigation system setup.

For this study, we reviewed our surgical cases that

were performed for pharmacoresistent focal epilepsy

using a neuronavigation device.

2. MATERIALS AND METHODS

In our retrospective study, we gathered the clinical data

of all patients who had navigation assisted surgery for

medically intractable epilepsy. We evaluated the charts

of 41 patients who were treated in our institution from

09.2003 to 08.2009 and reviewed the postoperative

clinical follow up as well as neuro-imaging data for the

degree of resection and complications.

Initially we used the Optical Tracking System (OTS®,

Radionics, Burlington, Massachusetts, USA). In 31 cases,

we navigated with the BrainLAB® System (BrainLAB,

Heimstetten, Germany) and in a further 9 cases with the

SonoWand® (Mison, Trondheim, Norway).

In frameless Neuronavigation, after general anaesthe-

sia has been induced and immediately before surgery the

patient’s head is fixed in a three point fixation device

and then referenced to the presurgical MRI (or other

imaging modality such as computed tomography) by

indicating to at least 4 defined landmarks so that the

navigation system may locate the patient´s head in the

three dimensional space. Hereafter the patient´s individ-

ual anatomy is shown on a monitor according to the re-

gion where a pointer is held on. The surgeon sees exactly

where the targeted lesion is in relation to the skull sur-

face to place the craniotomy on the ideal site. Moreover,

he may check the position of his instrument any time

during surgery.

For selective amygdala-hippocampectomies, we used

a supraorbital craniotomy via a subfrontal approach [19].

Temporal pole resections with amygdala-hippocampec-

tomies were approached via a small anterior temporal

craniotomy (diameter approx. 2.5 cm). For extratempo-

ral lesionectomies neuronavigation was also employed to

gain direct access with craniotomies as small as possible.

“Keyhole” approaches were applied when possible, es-

pecially in deeper seated lesions.

3. PATIENTS

This series includes 41 consecutive patients with phar-

macoresistent focal epilepsy with a mean age of 36 years

(15-70 years). There were 17 male and 24 female indi-

viduals. The mean duration of the epilepsy was 15.8

years. Most patients suffered from mesial temporal lobe

epilepsy (n = 28, 17 left/11 right). All of them had been

transferred from the department of neurology of the

University Medical Center, Mainz, after video-EEG-

monitoring for identification of the seizure onset region,

M. B. Glaser et al. / HEALTH 2 (2010) 753-758

755

correlation with the neuro-imaging and neuropsycholo-

gical testing. Histological findings showed hippocampal

sclerosis in 21 specimens. The remaining 7 had no spe-

cific changes (no abnormality, dysplasias, corpora amy-

lacea).

The extra-temporomesial pathologies consisted of 4

gangliogliomas, 1 gangliocytoma, 2 astrocytomas, 1

oligoastrocytoma, 2 cavernomas, 1 gliosis after hemor-

rhage from an AVM, 1 dermoid and 1 meningeoma (6

left/7 right).

4. SURGICAL PROCEDURES

The surgery for the mesial temporal lobe epilepsy pa-

tients consisted of 2 selective amygdalahippocampecto-

mies via a supraorbital subfrontal approach. The re-

maining 27 cases had an anterior temporal craniotomy

for pole resection and amygda l ah i pp ocampectomy.

The extratemporal pathologies were approached by

the shortest or least traumatic way concerning the pa-

tient´s neurological function. On the BrainLAB planning

station, it is possible to determine the trajectory and im-

port the information of the presurgical MRIs into the

intraoperative surgical field.

In the operating room neuronavigation was installed

after fixation of the patient’s head in the Mayfield clamp.

Accuracy was checked by correlation with anatomical

Figure 2. View of the hippocampus through the navigated

microscope.

landmarks after referencing the patients head with the

preoperative 3-D-MRI data set either by laser or land-

mark registration (at least 4 points; mostly nasion, lateral

orbital rims and upper helix attachments).

Neuronavigation was used to gain direct access to the

pathological structures. This was achieved generally by

use of a pointer. Additionally the microscope (Pentero or

NC4, Carl Zeiss, Oberkochen, Germany) itself could be

registered and navigated with the BrainLAB system. It

was especially helpful in the amygdala-hippocampec-

tomies in opening the temporal horn of the lateral ven-

tricle to enable the dissection of the hippocampus. The

viewing direction could be brought in the planned tra-

jectory to reach the targeted structure. When the target is

displayed in the ocular of the microscope, it is not nec-

essary for the surgeon to place a pointer in the surgical

field and look up to the monitor of the navigation sys-

tem.

Finally the neuronav igation was then used to “define”

the extent of resection of the hippocampus. It was in-

tended to remove it at least to the dorsal edge of the

cerebral peduncle.

5. DATA EVALUATION/FOLLOW UP

For all patients, site of surgery, duration between com-

pleted anaesthesiological preparation and skin incision

as well as the time for the surgery itself, blood loss, ICU

stay, hospital stay, neurological detoriation after surgery,

degree of resection and seizure outcome were collected.

The follow up of the patients and the classification

concerning Engel’s epileptological outcome classes [20]

were provided by the referring neurological department

(KJW). Mean follow up time was 23 month.

6. RESULTS

Installation and usage of the neuronavigation systems

was possible in all procedures. Average patient prepara-

tion (positioning, head fixation, referencing the neuro-

navigation, shaving, skin prepping, sterile draping) took

37 minutes. Mean duration of surgery was 209 minutes

from skin incision to wound closure. The mean ICU stay

scored 20.3 hours, the mean hospital stay 8.5 days.

There was an average blood loss of 310 cc per co mplete

procedure. Not a single bl ood pr o duct was ad ministered.

There was no mortality in this series. The following

complications were noted: One patient had a space oc-

cupying frontal epidural haematoma on his routine

postoperative cranial computed tomogram which was

clinically asymptomatic but evacuated for its size. Two

patients showed a slight hemiparesis caused by small

thalamic ischemias. They regained full strength but still

M. B. Glaser et al. / HEALTH 2 (2010) 753-758

756

have a deficit in fine motor skills. A further two patients

had incomplete oculomotor palsies which resolved

without sequelae. One patient developed a severe gener-

alized vasospasm 10 days after subtotal frontal lobec-

tomy. He has no focal neurological deficit but a relevant

lack of motivation.

One rhinoliquorrhoea occurred after a supraorbital

approach via the opened frontal sinus. The liquorrhoea

ceased after temporary lumbar drainage.

Postsurgical imaging showed complete removal of the

extratemporal pathologies in 9 of the 13 cases. The de-

gree of hippocampal resection was noted in relation to

the brain stem: a relatively short resection of the hippo-

campus only to the middle of the cerebral peduncle was

performed in 5 cases, to the dorsal margin of the cerebral

peduncle in 20 cases and in a further 3 cases beyond.

The neuronavigation was sufficiently exact in all

cases at the beginning of the procedure. Accuracy was as

reliable with laser patient registration as with registration

via anatomical landmarks. The calculated mean devia-

tion was 1.7 mm. It was possible to reach all lesions/

structures that were aimed for. It was extremely helpful

in localization of the temporal horn in amygdala-hippo-

campectomies. Neuronavigation overestimated the de-

gree of resection of the hippocampus, possibly due to

brain shift after CSF loss-especially after opening of the

lateral ventricle.

Postoperative seizure outcome was favourable after

amygdala-hippocampectomy with 21 patients Engel’s

class I and 6 patients Engel’s class II. One patient was

seizure free for 3.5 years and developed pharmacoresis-

tent temporal lobe epilepsy again so that re-resection is

being considered.

In the patients group with the extratemporal resections,

11 patients became seizure free (Engel’s class I). Two

patients did not profit at all and have still the same sei-

zure frequency in comparison to the presurgical state

(partial tumor resections).

In total, antiepileptic drugs were discon tinued in 8 pa-

tients and reduced in 5. The majority of 29 patients is

still under medication, similar to presurgical status.

7. DISCUSSION

For decades, atraumatic surgery for medically refractory

epilepsy has been the objective in order to improve pa-

tients functions and at the same time effectively reduce

seizures. Neuronavigation contributes to that aim by

minimizing the craniotomies and reach the target in the

planned trajectory [13].

On the other hand, there are only few publications

concerning neuronavigation and resective epilepsy sur-

gery [17,21-25].

Previous reports on neuronavigation in epilepsy sur-

gery were published without discussing its advantages

and pitfalls or without giving any clinical data [26-28].

Wurm et al. [24] published the largest series of 140

patients who underwent surgery for medically intractable

epilepsy. After the procedure for miscellaneous patholo-

gies surgeons answered a questionnaire to assess the

impact of the neuronavigation. They concluded that the

application of the navigation system was effectively and

safe in terms that the targets, even small in size, could be

located precisely and electrodes could be placed accu-

rately as well. Moreover the approach could be indi-

vidually tailored.

In a previous series of Oertel et al. [22] neuronaviga-

tion seemed to be helpful in avoidance of complications

(8% vs. 22%). In 93% the surgeon rated the application

of the neuronavigation as “helpful”.

A comparison of the complications in various studies

is compiled in Table 2, seizure outcome in Table 3.

In our series complication rate and seizure outcome

are comparable to larger series [29]. The application was

safe. There were no complications with direct referral to

the use of the navigation system. The time for prepara-

tion of the navigation was acceptable: in our evaluation

the total time from anaesthesia induction to skin incision

was 37 minutes. In comparison to that the installation of

the neuronavigation equipment alone took additional 26

minutes in another study [30]. Surgery itself was not

prolonged.

Table 1. Usefulness of neuronavigation.

Presurgical pla nni ng /st rategy Helpful for studying patients indiv idual anatomy

Determination of craniotomy si te Helpful, especially over convexity

Locating lesions Helpful, especially in subcortical p ath olo gie s

Amygdala-hippocam pectomies Extreme helpful in access the temporal horn

Resection control Var i a ble (brain shift), often overestimation, consider alternatives ( e.g. ultr asound )

Delicate site of surgery Helpful, shows eloquent structu res as well

M. B. Glaser et al. / HEALTH 2 (2010) 753-758

757

Table 2. Epilepsy surgery and complications (perm. = permanent; trans. = transient).

Complications Acar et al. Oertel et al. Cho et al. Glaser et al. Sindou et al. without Navigation

CSF fistula 2 trans. 1 trans.

Visual field defects 4 perm. Not investigated 1 4 perm. Not investigated

CN palsy 1 trans. 2 trans.

Motor deficit 1 perm. 1 trans. 2 trans. 2 perm.

Aphasia 1 trans. 1 perm. 1 trans.

Postop. haematoma 1 1 3

Infection 3

n = 39 n = 38 n = 46 n = 41 n = 100

Table 3. Seizure-outcome after epilepsy surgery.

Engel’s class Acar et al. Oertel et al. Cho et al. Glaser et al. Sindou et al. without Navigation

I 37 (95%) 20 (53%) 28 (61%) 32 (78%) 85 (85%)

II 2 (5%) 10 (22%) 4 (10%) 9 (9%)

III 6 (13%) 2 (5%) 2 (2%)

IV 2 (4%) 3 (7%) 4 (4%)

n = 39 n = 38 n = 46 n = 41 n = 100

8. CONCLUSIONS

Based on these results and our experience in the use of

neuronavigation, we conclude that the application of a

navigation system in epilep sy cases is safe and helpful in

finding the targeted structure and in minimizing trauma

to the patient by smaller craniotomies.

REFERENCES

[1] Hauser, W.A., Annegers, J.F. and Kurland, L.T. (1991)

Prevalence of epilepsy in Rochester, Minnesota: 1940-

1980. Epilepsia, 32(4), 429-445.

[2] Olafsson, E., Ludvigsson, P., Gudmundsson, G., Hes-

dorffer, D., Kjartansson, O. and Hauser, W.A. (2005) In-

cidence of unprovoked seizures and epilepsy in Iceland

and assessment of the epilepsy syndrome classification:

A prospective study. The Lancet Neurology, 4(10), 627-

634.

[3] Semah, F., Picot, M.C., Adam, C., Broglin, D., Arzi-

manoglou, A., Bazin, B., Cavalcanti, D. and Baulac, M.

(1998) Is the underlying cause of epilepsy a major prog-

nostic factor for recurrence? Neurology, 51(5), 1256-

1262.

[4] Kloster, R. and Engelskjon, T. (1999) Sudden unexpected

death in epilepsy (SUDEP): A clinical perspective and a

search for risk factors. Journal of Neurology, Neurosur-

gery & Psychiatry, 67(4), 439-444.

[5] Sillanpaa, M. and Schmidt, D. (2006) Natural history of

treated childhood-onset epilepsy: Prospective, long-term

population-based study. Brain, 129(Pt3), 617-624.

[6] Tonini, C., Beghi, E., Berg, A.T., Bogliun, G., Giordano,

L., Newton, R.W., Tetto, A., Vitelli, E., Vitezic, D. and

Wiebe, S. (2004) Predictors of epilepsy surgery outcome:

A meta-analysis. Epilepsy Research, 62(1), 75-87.

[7] Berg, A.T., Vickrey, B.G., Langfitt, J.T., Sperling, M.R.,

Walczak, T.S., Shinnar, S., Bazil, C.W., Pacia, S.V. and

Spencer, S.S. (2003) The multicenter study of epilepsy

surgery: Recruitment and selection for surgery. Epilepsia,

44(11), 1425-1433.

[8] Zernov, D. (1890) L’encephalometre. revue générale de

clinique et de thérapeutique, 19, 320.

[9] Horsley, V.R.C. (1908) The structure and functions of the

cerebellum examined by a new method. Brain, 31(1),

45-124.

[10] Kirschner, M. (1933) Die Punktionstechnik und die Elek-

trokoagulation des Ganglion Gasseri. Über gezielte Op-

erationen. Langenbecks Archiv für klinische Chirurgie,

176, 581-620.

[11] Grunert, P., Darabi, K., Espinosa, J. and Filippi, R. (2003)

Computer-aided navigation in neurosurgery. Neurosur-

gical Review, 26(2), 73-99.

[12] Enchev, Y. (2009) Neuronavigation: Geneology, reality,

and prospects. Neurosurgical Focus, 27(3), E11.

[13] Ganslandt, O., Behari, S., Gralla, J., Fahlbusch, R. and

Nimsky, C. (2002) Neuronavigation: Concept, techniques

M. B. Glaser et al. / HEALTH 2 (2010) 753-758

758

and applications. Neurol India, 50(3), 244-255.

[14] Wagner, W., Gaab, M.R., Schroeder, H.W. and Tschilt-

schke, W. (2000) Cranial neuronavigation in neurosur-

gery: Assessment of usefulness in relation to type and

site of pathology in 284 patients. Minim Invasive Neuro-

surg 43(3), 124-131.

[15] Spetzger, U., Laborde, G. and Gilsbach, J.M. (1995)

Frameless neuronavigation in modern neurosurgery.

Minim Invasive Neurosurg, 38(4), 163-166.

[16] Winkler, D., Lindner, D., Strauss, G., Richter, A., Schober,

R. and Meixensberger, J. (2006) Surgery of cavernous

malformations with and without navigational support-a

comparative study. Minimally Invasive Neurosurgery,

49(1), 15-19.

[17] Stone, S.S. and Rutka, J.T. (2008) Utility of neuronaviga-

tion and neuromonitoring in epilepsy surgery. Neurosur-

gical Focus, 25(3), E17.

[18] Nimsky, C., Ganslandt, O., Hastreiter , P., Wang, R., Benner,

T., Sorensen, A.G. and Fahlbusch, R. (2005) Preoperative

and intraoperative diffusion tensor imaging- based fiber

tracking in glioma surgery. Neurosurgery 56(1), 130-137.

[19] Reisch, R., Stadie, A., Kockro, R., Gawish, I., Schwandt,

E. and Hopf, N. (2009) The minimally invasive supraor-

bital subfrontal key-hole approach for surgical treatment

of temporomesial lesions of the dominant hemisphere.

Minim Invasive Neurosurg, 52(4), 163-169.

[20] Engel, J.V.N.P. Jr., Rasmussen, T.B. and Ojemann, L.M.

(Ed.), (1993) Outcome with respect to epileptic seizures.

Raven Press, New York.

[21] Miyagi, Y., Shima, F., Ishido, K., Araki, T., Taniwaki, Y.,

Okamoto, I. and Kamikaseda, K. (2003) Inferior tempo-

ral sulcus approach for amygdalohippocampectomy gui-

ded by a laser beam of stereotactic navigator. Neurosur-

gery 52(5), 1117-1123.

[22] Oertel, J., Gaab, M.R., Runge, U., Schroeder, H.W.,

Wagner, W. and Piek, J. (2004) Neuronavigation and

complication rate in epilepsy surgery. Neurosurgical Re-

view, 27(3), 214-217.

[23] Wurm, G., Wies, W., Schnizer, M., Trenkler, J. and Holl,

K. (2000) Advanced surgical approach for selective amy-

gdalohippocampectomy through neuronavigation. Neu-

rosurger y, 46(2), 1377-1382.

[24] Wurm, G., Ringler, H., Knogler, F., Schnizer, M. (2003)

Evaluation of neuronavigation in lesional and non-le-

sional epilepsy surgery. Computer Aided Surgery, 8(4),

204-214.

[25] Hirabayashi, H., Chitoku, S., Hoshida, T. and Sakaki, T.

(1999) Accuracy and availability of the computed as-

sisted neurosurgery navigation system during epilepsy

surgery. Stereotact Funct Neurosurg, 72(2-4), 117-124.

[26] Acar, G., Acar, F., Miller, J., Spencer, D.C. and Burchiel,

K.J. (2008) Seizure outcome following transcortical se-

lective amygdalohippocampectomy in mesial temporal

lobe epilepsy. Stereotact Funct Neurosurg, 86(5), 314-

319.

[27] Fahlbusch, R., Ganslandt, O. and Nimsky, C. (2000) In-

traoperative imaging with open magnetic resonance im-

aging and neuronavigation. Child’s Nervous System,

16(10-11), 829-831.

[28] Wheatley, B.M. (2008) Selective amygdalohippocam-

pectomy: The trans-middle temporal gyrus approach.

Neurosurg Focus, 25(3), E4.

[29] Sindou, M.G.M., Isnard, J., Ryvlin, P., Fischer, C. and

Mauguière, F. (2006) Temporo-mesial epilepsy surgery:

outcome and complications in 100 consecutive adult pa-

tients. Acta Neurochir (Wien), 148(1), 39-45

[30] Willems, P.W.A., Taphoorn, M.J.B., Burger, H., van der

Sprenkel, J.W.B. and Tulleken, C.A.F. (2006) Effective-

ness of neuronavigation in resecting solitary intracerebral

contrast-enhancing tumors: A randomized controlled trial.

Journal of Neurosurgery, 104(3), 360-368.