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Treatment of cavernous malformations in supratentorial eloquent areas: experience after 10 years of patient-tailored surgical protocol

  • Original Article - Neurosurgery general
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Eloquent area surgery has become safer with the development of intraoperative neurophysiological monitoring and brain mapping techniques. However, the usefulness of intraoperative electric brain stimulation techniques applied to the management and surgical treatment of cavernous malformations in supratentorial eloquent areas is still not proven. With this study, we aim to describe our experience with the use of a tailored functional approach to treat cavernous malformations in supratentorial eloquent areas.

Methods

Twenty patients harboring cavernous malformations located in supratentorial eloquent areas were surgically treated. Individualized functional approach, using intraoperative brain mapping and/or neurophysiological monitoring, was utilized in each case. Eleven patients underwent surgery under awake conditions; meanwhile, nine patients underwent asleep surgery.

Results

Total resection was achieved in 19 cases (95%). In one patient, the resection was not possible due to high motor functional parenchyma surrounding the lesion tested by direct cortical stimulation. Ten (50%) patients presented transient neurological worsening. All of them achieved total neurological recovery within the first year of follow-up. Among the patients who presented seizures, 85% achieved seizure-free status during follow-up. No major complications occurred.

Conclusions

Intraoperative electric brain stimulation techniques applied by a trained multidisciplinary team provide a valuable aid for the treatment of certain cavernous malformations. Our results suggest that tailored functional approach could help surgeons in adapting surgical strategies to prevent patients’ permanent neurological damage.

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Abbreviations

EBS:

Electric brain stimulation

CM:

Cavernous malformation

DTI:

Diffusion tensor imaging

fMRI:

Functional magnetic resonance imaging

IONM:

Intraoperative neurophysiological monitoring

MRI:

Magnetic resonance imaging

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Author information

Authors and Affiliations

  1. Neurosurgery Department, Hospital Universitari de Bellvitge, Feixa Llarga s/n, 09807, Hospitalet de Llobregat, Barcelona, Spain

    Jose L. Sanmillan, Pablo Lopez-Ojeda, Alejandro Fernández-Coello, Gerard Plans & Andreu Gabarrós

  2. Neurophysiology Department, Hospital Universitari de Bellvitge, Feixa Llarga s/n, 09807, Hospitalet de Llobregat, Barcelona, Spain

    Isabel Fernández-Conejero

  3. Universitat de Barcelona, C/ Casanova 143, 08036, Barcelona, Spain

    Yara Ali-Ciurana

Authors
  1. Jose L. Sanmillan
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  2. Pablo Lopez-Ojeda
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  3. Isabel Fernández-Conejero
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  4. Alejandro Fernández-Coello
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  5. Gerard Plans
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  6. Yara Ali-Ciurana
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  7. Andreu Gabarrós
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Correspondence to Jose L. Sanmillan.

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Conflict of interest

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge, or beliefs) in the subject matter or materials discussed in this manuscript.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Comments

The authors present their 10-year surgical experience on cavernous malformation resection with an individualized functional approach using preoperative functional study (fMR and DTI tractography) and intra-operative brain mapping and/or neurophysiological monitoring with awake (11 patients) or asleep (9 patients) surgery. We must congratulate with JL Sanmillan and co-workers because of their remarkable results since they achieved a high resection rate and high seizure control with a low morbidity rate on selected patient population affected by a cavernoma located in an eloquent area.

The issue is remarkable because surgical treatment of cavernous malformations (CMs) in eloquent areas is challenging, and there is an interesting debate in the scientific community about two specific issues when dealing with this subgroup of cavernomas: What should be the indication-to-treat policy and how surgery should be performed when treatment has been planned. For this reason, new data on treatment results and on new approaches are welcome.

We are pleased to get to the heart of the matter with some considerations. First, we agree with the authors about the indication-to-treat policy based on cavernoma features (growing at follow-up, cause of symptoms, or drug-resistant epilepsy) rather than on cavernoma location. However, we must highlight that this policy was possible to the authors because they adopted a functional approach that allowed them to have a low morbidity although operating into crucial areas. Second, we agree with the authors that an intra-operative functional approach is unavoidable when dealing with cavernoma located into or close to an eloquent area; frankly, we think that sometimes preoperative functional imaging can be misleading. As a matter of fact, the authors showed that in 20% of reported cases, surgical strategy had to be changed based on intra-operative brain stimulation findings. To this purpose, we would like to emphasize that brain mapping in cavernoma surgery is crucial not only for the well-known brain shift during surgery but also especially because of unreliability of DTI data in strict proximity of cavernoma to track functional pathway due to artifacts related to hemosiderin surrounding cavernoma. This must be carefully kept in mind when resection of hemosiderin ring around cavernoma is planned. Third, we completely agree with the authors that hemorragic cavernoma in eloquent areas should be removed as soon as possible. We have recently managed the case of a patient affected by an hemorragic cavernoma located close to Broca area presenting with a slight speech disturbance which we planned to postpone surgery to operate on her later, in awake surgery, as far as her language would have recovered. One month after, first bleeding patient presented a second bleeding. She underwent emergent resection in asleep surgery. Fortunately, she finally did not report permanent language disturbances.

We would like to report some further technical considerations arising from our surgical experience on supratentorial cavernoma:

Our policy is to always remove hemosiderin ring surrounding cavernoma, even in non-epileptic patients, when functionally possible. This approach frequently implies perilesional tissue resection larger than expected; thus, we think that neurophysiological monitoring is mandatory even when cavernoma is more distant than 1 cm from a functional area/pathway

In approaching cavernoma located into the parietal areas, we experienced awake surgery not only aiming at language but also at calculation (one case) and at visuo-spatial (one case) intra-operative assessment. Neglect and acalculia remain an underestimated cause of reduced quality of life in patients undergoing surgery in parietal areas. In both patients, explored function was preserved by a surgical injury.

We suggest to charge into the neuronavigation system two MR sequences: one with the aim to track cavernoma (usually T1-weighted images) and the other with the aim to track hemosiderin ring (usually T2 or SWI-weighted images). Although SWI can be limited by the so-called blooming artefact, we experienced a high utility in planning corticotomy based on SWI images charged into neuronavigation system.

Hemosiderin ring can be removed by using CUSA that can allow gentle removal of perilesional healthy tissue, while motor/language pathway can be traced by exploiting the stimulation effect carried out by the ultrasonic device. This approach is well known and widely used in glioma surgery.

An emerging intra-operative tool in CM surgery is ICG-videoangiography. In our experience, it was useful to identify venous malformation, often associated to and in intimate relation with cavernoma.

Some considerations about future perspective in this field of neurosurgery:

1. It would be interesting to test resting state MR (rsMR) application in patients affected by a cavernoma located in an eloquent area when function at risk is not sufficiently assessable at preoperative and intra-operative evaluation.

2. Brain plasticity in cavernoma patients has been not deeply investigated. As the authors interestingly reported in the case with incomplete CM resection, this approach could potentially allow a safer late repeated surgery.

Domenico d’Avella

Alessandro Della Puppa

Padova, Italy

This article is part of the Topical Collection on Neurosurgery General

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Sanmillan, J.L., Lopez-Ojeda, P., Fernández-Conejero, I. et al. Treatment of cavernous malformations in supratentorial eloquent areas: experience after 10 years of patient-tailored surgical protocol. Acta Neurochir 160, 1963–1974 (2018). https://doi.org/10.1007/s00701-018-3644-3

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