Augmented reality (AR) in microsurgical multimodal image guided focal pediatric epilepsy surgery. A technical note

doi:10.21203/rs.3.rs-4973438/v1

Background: Augmented reality (AR) is increasingly being used to improve surgical planning and assist in real time surgical procedures. A retrospective investigation was conducted to study its role in pediatric epilepsy surgery at a single institution.

Methods: Functional neuronavigation using multimodal imaging data (fMRI, DTI-tractography, PET, SPECT, sEEG) were used to augment the surgical navigation by transferring 3D imaging reconstructions as AR maps into the surgical microscope overlaying the surgical field.

Results: Altogether, 43 patients (17 female, 0-18 yrs, mean 9 yrs) were operated between 10/2020 and 10/2023 and fulfilled the inclusion criteria. 26 patients (60.5%) had an extra-temporal and 17 (39.5%) a temporal seizure origin. The 3 top histological diagnoses were : FCD (32.6%), ganglioglioma (23.3%) and DNT (11.6%). Preoperative MRI studies showed no epileptogenic lesion in 11 patients (25.6%, MRI negativ group), which necessitated implantation of depth electrodes before resection. Altogether, of 25 patients with a follow up of more than one year, 83% displayed a favorable ILAE grade 1 seizure outcome (75% ILAE 1a). Altogether, 14% experienced a transient hemiparesis, 7% a quadrantanopia and one needed a subdural- peritoneal shunt.

Conclusion: AR supported microscope resection facilitated targeting and removal of lesional as well as non-lesional (sEEG defined) epileptogenic lesions in pediatric epilepsy surgery with low morbidity and a remarkably favourable seizure outcome.

Augmented reality

Image guided surgery

pediatric epilepsy surgery

Seizure outcome

Augmented reality (AR) is increasingly used for surgical education, but already also for guiding intraoperative surgical strategy in different fields of neurosurgery, like spine surgery, skull base surgery and vascular neurosurgery^1,4,7-9. In pediatric epilepsy surgery the definition of the epileptogenic zone (EZ), the brain tissue which has to be removed to render the patient seizure free, is still a challenge and needs multiple preoperative image investigations for definition of the surgical resection even in focal epilepsy⁵. Functional images created out of stereo- electro-encephalography (sEEG) results, positron emission tomography (PET), single-photon emission computer tomography (SPECT) and magnetoencephalography (MEG) may be directly used for image guided surgery (IGS). Therefore, images have to be overlayed on the surgical field for guiding the resection, typically using the microscope¹³. Additionally, augmented reality support can be performed by using instruments like a navigated suction device and the multicolor display of the surgical microscope to transfer image information on to the brain of the surgical field during resection, respectively. MRI scans including multimodal imaging information are used to augment the resection strategy further by displaying it additionally into the microscope.

However, the effectivity and results of such an augmented reality supported resection strategy in pediatric epilepsy surgery has not yet been investigated till now. Therefore, a retrospective study was performed to analyze the direct impact on completeness of the resections of lesions/ epileptogenic zones as well as on complications and the resulting seizure outcome.

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Institutional Review Board (or Ethics Committee) of Medical University of Vienna (EK Nr: 1542/2024, APRES Study- study on the effect of augmented reality in pediatric epilepsy surgery).

The Zeiss Kinevo Microscope (Zeiss, Oberkochen, Germany) allows the implementation of images into the microscope via a multicolor microscopical display. The Brainlab Navigation System (Brainlab, Munich, Germany) can be connected to the Zeiss microscope and used as a neuronavigation tool. In addition to providing resection contours, 3 D MRI images can be displayed in the microscopical eye piece and used for navigated resection. This allows the comparison of the resected brain tissue with the preplanned resection volume on the MRI images on-line by constantly looking through the microscope (Fig. 1) Additionally, the Brainlab Navigation allows to implement additional instruments as navigation tools for the resection, like a navigated suction device. For that study, the regular suction device (Neuromedics, Hamburg, Germany) was equipped with Brainlab tracking stars to use it as a navigation tool. The tip of the suction could also be displayed on the virtual reality images within the microscope and used for navigational guidance during resection.

Altogether, 43 patients (17 female, 0–18 yrs, mean 9 yrs) were operated between 10/2020 and 10/2023 and fulfilled the inclusion criteria. 26 patients (60.5%) had an extra-temporal and 17 (39.5%) a temporal seizure origin. Preoperative MRI studies were negative for lesions in 11 patients (25.6%), which necessitated implantation of depth electrodes before resection. The 3 top histological diagnoses were : FCD (32.6%), ganglioglioma (23.3%) and DNT (11.6%) (Table 1).

Advantages of AR augmentation were: 1. on-line targeting of the lesions and visualisation of eloquent brain areas next to the lesion, 2. By using this method, avoiding injury of eloquent brain structures, 3. contour-guided resection of lesions even in cases with unclear visual delineation according to sEEG spatial information, and 4. estimation of the resection amount at the end of surgery.

Altogether, of 25 patients with a follow up of more than one year, 83% displayed a favorable seizure outcome with ILAE 1 (with 75% beeing completely seizure free since the surgery- ILAE 1a).

Altogether, 6 patients experienced a transient hemiparesis which resolved within the next 3 months (14%), 3 patients had a permanent upper quadrantanopia at the contralateral side to the surgery (7%) and one patient needed a subdural- peritoneal shunt because of progredient subdural hematoma (2%). No acute complications leading to surgical revision were encountered.

Augmented reality (AR) real time surgical neuronavigation proofed to be beneficial in this retrospective study to achieve outstanding rates of seizure free pediatric patients after brain surgery of focal drug-resistant pediatric epilepsy. Altogether, 83% of patients with a FU of more than one year operated for drug resistant seizures achieved a favorable seizure outcome ILAE Class1, 75% ILAE 1a.

Transferring image information on to the surgical field for online- neuronavigational guidance using AR is a new development adapted from neurosurgical training and surgical interventions in other fields of surgery.¹⁴ Recently, operating microscopes can be equipped with navigation tools and polychromatic displays for implementing multimodal image information and 3plane MRI images. This allows on-line targeting of the epileptic lesions and epileptic foci defined by depth electrodes in the investigated drug resistant pediatric epilepsy patients in this study. Targeting the lesions with contour guidance via the polychromatic microscope display was already successfully used by the authors who have pioneered this field in the past^11,12.

But augmenting the resection by virtual reality images within the microscope is a new development now successfully and routinely applied during pediatric epilepsy surgery in the last few years at the institution.

Not only on-line targeting of lesions became safely available, but also sparing eloquent brain areas outlined in the neuronavigational images displayed virtually within the eyepiece of the microscope lead to avoid complications. Accordingly, no severe complications and no revision surgery are reported in this retrospective study of 43 patients.

The main advantages were the online targeting of the lesions as well as image/ sEEG defined EZs, avoiding complications by including eloquent image information like motor- and speech MRI as well as memory areas. This AR conducted surgery allowed resection of affected tissue without obvious haptic differentiation and estimation of the resection amount at the end of surgery.

All different advantages are not newly described for resection strategies using neuronavigation systems and image- guided surgery¹⁰, but the implementation of augmented reality by using the 3D MRI images as direct feedback during resection is a new approach and has not been described for pediatric epilepsy surgery till now.

The complication rate was extremely low in this series compared to the literature (0% permanent motor or speech deficits, 14% temporary hemiparesis, 7% upper quadrantanopia and 2% shunt implantation) ², contrasting with a seizure outcome which was exceptional good^3,6, especially when considering that 2/3 of the patients had extratemporal pathologies and ¼ were MRI negative epileptic zones defined by sEEG.

AR supported image guided navigated microscope resection facilitated targeting and removal of lesional as well as non-lesional (sEEG defined) epileptogenic zones in pediatric epilepsy surgery with low morbidity and a remarkably good seizure outcome.

AR	Augmented reality
DTI	Diffusion tensor imaging
DIG/DIA	Desmoplastic infantil ganglioglioma/astrocytoma
DNT	Dysembryioplastic neuroepithelioma
EZ	Epileptogenic zone
FCD	Focal cortical dysplasia
fMRI	Functional magnetic resonance tomography
GG	Ganglioglioma
HS	Hippocampal sclerosis
IGS	Image guided surgery
ILAE	International league against epilepsy
mMCD	Mild malformation of cortical development
MOGE	Mild malformation of cortical development with oligodendroglial hyperplasia
MEG	Magnetoencephalography
MRI	Magnetic resonance tomography
PET	Positron emission tomography
sEEG	Stereo encephalography
SPECT	Single photon emission computer tomography
SEGA	Subependymal giant astrocytoma

Author Contributions: “Conceptualization, R.K.; methodology, R.K., J.S.; validation, R.K., J.S., M.T., F.M.; formal analysis, F.W..; investigation, X.X.; resources, K.R., M.F.; data curation, M.F.; writing—original draft preparation, J.S., K.R..; writing—review and editing, K.R., M.F..; visualization, K.R., J.S..; supervision, K.R. and C.D., All authors have read and agreed to the published version of the manuscript.

Funding: “This research received no external funding”

Institutional Review Board Statement: The study was conducted in accordance with the Declaration of Helsinki, and approved by the Institutional Review Board (or Ethics Committee) of Medical University of Vienna (EK Nr: 1542/2024, APRES Study)).

Acknowledgments: We would like to thank all individuals who contributed to the study or manuscript preparation but did not meet all the criteria for co-authorship.

Conflicts of Interest: The authors declare no conflict of interest.

Begagic E, Beculic H, Pugonja R, Memic Z, Balogun S, Dzidic-Krivic A et al (2024) Augmented Reality Integration in Skull Base Neurosurgery: A Systematic Review. Med (Kaunas) 60
Behrens E, Schramm J, Zentner J, Konig R Surgical and neurological complications in a series of 708 epilepsy surgery procedures. Neurosurgery 41:1–9; discussion 9–10, 1997
Englot DJ, Breshears JD, Sun PP, Chang EF, Auguste KI (2013) Seizure outcomes after resective surgery for extra-temporal lobe epilepsy in pediatric patients. J Neurosurg Pediatr 12:126–133
Fabrig OD, Serra C, Kockro RA (2024) Virtual Reality Planning of Microvascular Decompression in Trigeminal Neuralgia: Technique and Clinical Outcome. J Neurol Surg A Cent Eur Neurosurg
Gong R, Bickel S, Tostaeva G, Lado FA, Metha AD, Kuzniecky RI et al (2024) Optimizing Surgical Planning for Epilepsy Patients With Multimodal Neuroimaging and Neurophysiology Integration: A Case Study. J Clin Neurophysiol
Guo J, Wang Z, van 't Klooster MA, Van Der Salm SM, Leijten FS, Braun KP et al (2024) Seizure Outcome After Intraoperative Electrocorticography-Tailored Epilepsy Surgery: A Systematic Review and Meta-Analysis. Neurology 102:e209430
Halpin BS, Patra DP, Chavarro V, Bendok BR (2024) Virtual Planning and Augmented Reality-Guided Microsurgical Resection of a Frontal Arteriovenous Malformation. World Neurosurg 185:245
Judy BF, Menta A, Pak HL, Azad TD, Witham TF (2024) Augmented Reality and Virtual Reality in Spine Surgery: A Comprehensive Review. Neurosurg Clin N Am 35:207–216
Nguyen L, Bordini M, Matava C (2024) Using Virtual Reality for Perioperative Nursing Education in Complex Neurosurgical Surgeries: A Feasibility and Acceptance Study. Cureus 16:e55901
Roessler K, Hofmann A, Sommer B, Grummich P, Coras R, Kasper BS et al (2016) Resective surgery for medically refractory epilepsy using intraoperative MRI and functional neuronavigation: the Erlangen experience of 415 patients. Neurosurg Focus 40:E15
Roessler K, Ungersboeck K, Aichholzer M, Dietrich W, Goerzer H, Matula C et al Frameless stereotactic lesion contour-guided surgery using a computer-navigated microscope. Surg Neurol 49:282–288; discussion 288–289, 1998
Roessler K, Ungersboeck K, Czech T, Aichholzer M, Dietrich W, Goerzer H et al (1997) Contour-guided brain tumor surgery using a stereotactic navigating microscope. Stereotact Funct Neurosurg 68:33–38
Roessler K, Winter F, Kiesel B, Shawarba J, Wais J, Tomschik M et al (2024) Current Aspects of Intraoperative High-Field (3T) Magnetic Resonance Imaging in Pediatric Neurosurgery: Experiences from a Recently Launched Unit at a Tertiary Referral Center. World Neurosurg 182:e253–e261
Zhou Y, Cai P, Zeng N (2024) Augmented reality navigation system makes laparoscopic radical resection of hilar cholangiocarcinoma type Ⅲb more precise and safe. J Gastrointest Surg

Table 1: Histological entities

Histology	Nb (%)
FCD	14 (32.6%)
GG	10 (23.3%)
DNT	5 (11.6%)
mMCD	3 (7.0%)
Gliosis	2 (4.7%)
MOGE	2 (4.7%)
DIG/DIA	1 (2.3%)
Encephalitis	1
Angiocentric Glioma	1
Astroblastoma	1
HS	1
SEGA/FCD2b	1
Cavernoma	1

Table 2: Seizure outcome diagnosis

Diagnosis	ILAE Class 1a

FCDs	8/10 (80%)
GGs	9/10 (90%)
DNETs	4/5 (80%)

No competing interests reported.

Augmented reality (AR) in microsurgical multimodal image guided focal pediatric epilepsy surgery. A technical note

Status:

Version 1

Abstract

Figures

Introduction

Materials and Methods

Results

Discussion

Conclusions

Abbriviations

Declarations

References

Tables

Additional Declarations

Status:

Version 1