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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 53  |  Issue : 3  |  Page : 135-145

Anatomical resection in glioblastoma: extent of resection and its impact on duration of survival


Department of Neurosurgery, Ain Shams University, Cairo, Egypt

Date of Submission03-Jan-2016
Date of Acceptance28-Mar-2016
Date of Web Publication27-Oct-2016

Correspondence Address:
Salah M Hamada
24, Dr. Soliman Azmy Street, Nozha, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


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  Abstract 

Introduction Glioblastoma is still a disease without a cure despite the use of a multimodal approach. The extent of resection has been the only modifiable factor in the different variables that affect survival. Cellular tumour infiltration beyond the visible enhancing excisable lesion remains the cornerstone for inevitable disease recurrence and progression.
Patients and methods We prospectively evaluated the impact of the extent of resection beyond the visible enhancing tumour on the survival. We evaluated 59 patients with glioblastoma who were operated upon by maximum possible safe excision of the tumour and the surrounding involved gyri or lobe as long it was not considered eloquent. We followed the patients until recurrence and death.
Results Fifty-nine patients, 43 men, mean age 48 years, were studied. Overall, 28.8% of the tumours were frontal, 20% were parietal, 37.2% were temporal and 14% were occipital. The median preoperative contrast-enhancing tumour volume was 42.36 ml. Twenty patients (34%) underwent anatomical excision, 21 patients (36%) underwent gross total excision, 14 patients (24%) underwent subtotal and four patients (7%) underwent surgical debulking. In all, 79.66% of the patients died. There was a statistically significant reduction in the mean survival with less aggressive resection, for which the average survival was 16.5 months for the anatomical resection group, 12.09 months for the gross total excision group, 7.34 months for the subtotal excision group and 4.67 months for the debulking group (P = 0.002).
Conclusion Total tumour resection with extra margin of tumour-infiltrated gliotic tissue, followed by adjuvant radiochemotherapy leads to longer survival than less radical excision.

Keywords: extent of resection, glioblastoma survival, glioblastoma


How to cite this article:
Hamada SM, Abou-Zeid AH. Anatomical resection in glioblastoma: extent of resection and its impact on duration of survival. Egypt J Neurol Psychiatry Neurosurg 2016;53:135-45

How to cite this URL:
Hamada SM, Abou-Zeid AH. Anatomical resection in glioblastoma: extent of resection and its impact on duration of survival. Egypt J Neurol Psychiatry Neurosurg [serial online] 2016 [cited 2021 Apr 19];53:135-45. Available from: http://www.ejnpn.eg.net/text.asp?2016/53/3/135/193063


  Introduction Top


Glioblastoma (GBM) is the most common and most aggressive primary brain tumour [1],[2],[3]. It is a disease without a cure [4]. The 5-year survival rate is about 4% [5]. The duration of survival has not changed much over the past few decades [6].

It represents about 15% of all intracranial neoplasms and 60–75% of astrocytic tumours [7]. The WHO abandoned the term multiforme and used the term glioblastoma; however, the term GBM is still in use in practice and the medical literature [1],[4],[8].

Histologically, GBM arises from astrocytes and is typically highly cellular, poorly differentiated with pleomorphic anaplastic cells that express nuclear atypia and has a high mitotic activity with a rich vascular supply and shows extensive necrosis [1],[9],[10],[11].

The clinical presentation is according to the tumour size and location, together with the degree of surrounding oedema [4], Upon initial presentation, the plain noncontrasted brain computed tomography (CT) remains the screening tool for the detection of tumourous intracranial pathology, and yet, when GBM is detected, high-resolution contrasted MRI should be performed [4].

The treatment of newly diagnosed GBM is through a multimodal approach with maximum possible safe resection, followed by adjuvant radiation therapy and chemotherapy [12],[13],[14],[15]. This multidisciplinary approach only results in a median overall survival of 9–22 months [12],[13],[14],[15].

Many factors affect the length of survival including age, Karnofsky performance scale (KPS), extent of resection (EOR), subtypes of GBM, methylation status of O-6-methylguanine-DNA methyltransferase and response to chemotherapy and radiation [16],[17],[18].

The aim of surgical management includes acquisition of tissue samples for histology, maximum possible tumour removal with the least possible morbidity and maintenance or improvement of the preoperative KPS with the aim of extending survival with the best possible quality of life [4].

Surgery, when feasible, remains the first line of treatment and according to current evidence, the extent of surgical resection is considered a key component of treatment and in achieving good results [19],[20],[21],[22],[23],[24],[25]. Numerous surgical adjuncts such as diffusion tensor imaging, functional MRI, intraoperative MRI (iMRI) and 5-aminolevulonic acid have proven efficacious in this respect [19].

However, even among patients who have undergone gross total resection (GTR), the median survival remains 11.2 months [6]; most of the deaths occur because of local tumour recurrence.

Despite the fact that many patients are operated upon by GTR, the median survival remains 11.2 months, with the most common cause of mortality being local tumour recurrence [6]. This might be attributed to the presence of tumour cells beyond the previously excised enhancing margin and within the surrounding oedema [20],[21],[22],[23].

When the tumour is far from the eloquent cortex or when the eloquent cortex has already been destroyed by tumour infiltration, we prefer super total excision (excision with a safety margin), where the tumour-infiltrated oedematous tissue surrounding the tumour is resected together with the tumour either by complete excision of the rest of the involved gyrus or by complete lobectomy of the anatomical territory involved.


  Patients and methods Top


This was a prospective cohort study of 59 patients who underwent craniotomy for GBM between October 2008 and July 2015, after approval of study protocol by ethical committee.

All patients were subjected to a thorough neurological examination and a contrasted preoperative MRI scan; in addition, some patients underwent functional imaging when the lesion was in proximity to the eloquent cortex and most patients underwent a CT scan of the brain at the onset of their symptoms.

We prescribed all patients with prophylactic intravenous antibiotics with induction of anaesthesia during their hospital stay and, on discharge, they were prescribed oral antibiotics for 3 more days.

We routinely administer prophylactic antiepileptic drugs perioperatively and gradually taper them after 2 weeks unless patients develop seizures, in which case we continue with the antiepileptic medications.

Patient were operated upon utilizing a standard craniotomy; the choice of a linear skin incision or a flap was made according to the expected area of exposure for craniotomy, which was either performed using manual instruments such as a gigli saw or an electric craniotome.

The dura was opened either a U shape or cruciate, with the base opposite the most eloquent side.

Following the initial corticotomy or gyrectomy, we initiate internal tumour debulking, initially by the naked eye or by loupe magnification, followed by the use of an operating microscope (Zeiss S88, Jena, Germany). We carry on with debulking until further identification of tumourous tissue is not possible, and then we re-evaluate the anatomy of the surgical field and correlate it with the preoperative radiology in an attempt to find residual tumour hidden ‘around the corner’ of the surrounding gliotic cortex or reidentify possible tumour tissue initially believed to be oedematous brain tissue.

After resection of all visible tumours, we classify the surrounding cortex as either noneloquent (e.g. inferior temporal gyrus), possibly eloquent (e.g. superior temporal gyrus) and definitely eloquent (e.g. posterior part of the frontal lobe). We then resect the rest of the involved gyrus if it is not definitely eloquent.

We categorized the EOR into four categories: anatomical resection (including the entire involved gyrus or lobe as applicable), GTR, subtotal resection and surgical debulking.

We close the dura in a watertight manner with application of a dural patch if required. We reposition the bone flap and secure it in place with absorbable heavy polyglycolic acid suture (Vicryl; Ethicon, Somerville, NJ, USA). We then close the skin flap in layers on a suction drain.

All patients were revived from anaesthesia and extubated in the theatre and then transferred to the ICU until they were vitally and neurological stable to be discharged to the wards [Figure 1],[Figure 2],[Figure 3],[Figure 4].
Figure 1: A case of right parietal glioblastoma.

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Figure 2: A case of left occipital glioblastoma.

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Figure 3: A case of right temporal glioblastoma.

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Figure 4: A case of right frontal glioblastoma with corpus callosum involvement.

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  Results Top


Our study was carried out on 59 patients: 43 men (73%) and 16 women (27%), mean age 48.57 ± 15.32 years (range 24–75 years). Seventeen (28.8%) tumours were frontal, 12 tumours (20%) were parietal, 22 tumours (37.2%) were temporal and eight tumours (14%) were occipital. Thirty-six patients (61%) had right-sided tumours 23 patients (39%) had tumours left-sided tumours. The most common presentations were headaches (78%), seizures (25%) and neurological deficits (56.%). Neurological deficits included language problems, visual field defects, and motor and sensory affection. Just over a third of the patients (39%) had associated non-neurological comorbidities, 7% presented with a disturbed level of consciousness, but wereall above Glasgow Coma Scale score of 9, and only five of our patients (8.47%) had a KPS less than 70%.

The median preoperative contrast-enhancing tumour volume was 42.36 ml; in terms of proximity to eloquent areas, 38 tumours (65%) were all within a noneloquent brain, 18 tumours (30%) were close to an eloquent brain and three tumours (5%) were within an eloquent brain.

Twenty patients (34%) underwent anatomical excision, 21 patients (36%) underwent gross total excision, 14 patients (24%) underwent subtotal and four patients (7%) underwent surgical debulking [Table 1].
Table 1: Tumours according to location and surgical management

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In the early postoperative period, all patients recovered from surgery and 17% had early postoperative seizures, which were generalized tonic–clonic and treated with medication; these patients were monitored in the ICU until they achieved complete recovery of level of consciousness. The mean duration for postoperative ICU admission was 2.8 days (1–10 days). We had no 30-day operative mortality in this series. Nine patients developed immediate postoperative new motor weakness that was not present preoperatively; all except two were transient and recovered within 2 weeks, and the remaining two patients had persistent weakness.

Seven patients had increased language problems, but all had initially transient partial dysfunction and recovered quite well over the following few weeks.

Two patients had completion of field defect that was present preoperatively and did not recover; however, the patients reported improved vision probably because of adaptation [Table 2].
Table 2: Duration between surgery and radiological detection of either recurrence or active progression of a residual tumor

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Although all patients had local recurrence or regrowth, we only reoperated on 20.25% of the patients. The patients who underwent only one operation either chose not to undergo an operation again or the direction of growth was deeper towards the inner structures; therefore, we decided not to operate.

Until the date of this research in November 2015, 47 of 59 patients, 79.66%, died.

There was a statistically significant reduction in the mean survival with less aggressive resection, where the average survival was 16.5 months for the anatomical resection group, 12.09 months for the gross total excision group, 7.34 months for the subtotal excision group and 4.67 months for the debulking group as shown in [Table 3] (P = 0.002) [Figure 5].
Table 3: Mean survival according to the extent of resection

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Figure 5: Kaplan–Meier survival curve showing significant survival benefit in favour of anatomical resections.

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  Discussion Top


All the advancements and developments in radiation oncology and chemotherapy are still not enough to provide a cure for patients with GBM. Current practice relies considerably on the surgical excision of this deadly tumour to improve quality survival in our patients [4],[6],[19].

Patients respond differently to the multimodal treatment strategy for GBM; this variable response may be attributed to intrinsic tumour characteristics such as methylation status of 6-methyl-guanine-DNA-methyltransferase and the presence of mutation of isocitrate dehydrogenase (IDH 1 gene) [24],[25].

Among the numerous determining factors, only the EOR is modifiable; all other factors are outside our circle of influence [19].

The previous concept that surgery should be performed just for decompression and not for reducing tumour burden [26],[27] is currently refuted. According to the current practice concepts, the extent of debulking or excision is significantly related to survival [6],[19],[28],[29], which is why the ‘as much as possible’ has replaced the ‘all or none’ concept for the surgical management of GBM [19].

Perioperative KPS is important in choosing surgical candidates with a higher than 90% chance of achieving a favourable outcome, provided that the surgery does not adversely affect the KPS or result in new neurological deficits. Patients with a KPS less than 70% are considered poor surgical candidates [18],[28],[30].

In our series, we believe that the improvement in KPS that occurred in some cases postoperatively may have been because of decompression of a previously compressed noninvaded brain as a result of tumour resection.

The anatomical relationship between the tumour and the eloquent cortex is pivotal as it is directly related to the amount of tumour that can be resected without permanent neurological disability [4]. Proximity to the eloquent cortex remains the strongest predictor for the ability to completely excise the tumour. Noneloquent cortex tumours are 11.8 times more likely to be excised than those located within the eloquent cortex [31].

Yet, we must keep in mind that the definition of eloquent versus noneloquent is changing constantly with rapidly progressing technologies, and understanding of functional imaging, voxel-based morphometry, fibre tracking and chemoarchitectonics show that areas that we previously believed to be noneloquent have been proved to be very useful if not a ‘functional centre’ yet to be part of a ‘ functional network’ [32],[33],[34].

We believe that careful planning, meticulous surgery and aggressive tumour excision are keys to achieving successful deficit-free prolonged survival.

In our practice, we encountered occasional difficulty in the intraoperative identification of tumour, especially at the margins. It might sometimes be challenging and attempts at excision of this equivocal tissue may be hazardous, especially in proximity to the eloquent cortex.

We attempted to overcome this limitation by anatomical identification of this equivocal location rather than assessing the gross pathological appearance of the tissue. If this location is found to be noneloquent and within the vicinity of the contrast-enhancing lesion, we perform excision by considering it either a tumour margin or surrounding infiltrated gyrus.

A careful preoperative radiological evaluation helps identify the delicate anatomical relationship between the tumour, the surrounding tumour cells embedded within an oedematous brain and the surrounding tumour-free brain and its relation to the functioning brain around.

We did not perform an intraoperative radiological evaluation, except in one patient by intraoperative ultrasound; thus, we had to reply completely on the surgeon’s skill whether to excise or not.

Currently, all surgical efforts are directed towards maximizing the EOR because of its confirmed prognostic value [6],[28],[35],[36]; the previous adoption of less aggressive resections resulted in patients being twice as likely to die during the early follow-up period [31].

Many studies have evaluated the EOR and its impact on survival; some did not use perioperative volumetric analysis [37],[38],[39] whereas only six recent studies used volumetric analysis [19]. All of these studies came to the same conclusion that the more the EOR, the longer quality survival, provided that surgery does not result in extra morbidity. The studies differed on the lower threshold for significant excision.

Lacroix et al. [28] concluded that a proportional increase in the duration of survival occurred with each unit increase in the EOR, starting from 89%, with the strongest effect of resection on survival being achieved at the 98% threshold. Sanai et al. [40] from UCSF reported significant survival advantage that started at 78% [Table 4].
Table 4: Details of survival according to lobe and surgery arranged from maximum mean survival to minimum

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In addition to the EOR, another variable is considered more important, which is the residual tumour volume (RV), as the EOR value is questionable compared with the amount of tumour left behind. Resection of 80% of a 100 ml tumour leaves behind 20 ml, whereas resection of 80% of 30 ml tumour leaves behind 6 ml tumour. It is definitely not the same tumour burden [19],[29],[42].

Chaichana and colleagues reported that a maximum RV of 5 ml represents the statistical cutoff for improving progression-free survival. The higher the residual volume, the higher the remaining tumour cells that are resistant to adjuvant therapy [42]. Grabowsky et al. [29] reduces the volume to just 2 ml for it to impact improved survival positively.

From all the previous discussions, we reach two irrefutable conclusions: the more we remove, the longer the survival and that the tumour cells invade the surrounding milieu of the contrast-enhancing lesion. Therefore, if possible, we should definitely surgically remove all existing tumour cells whether within the contrast-enhancing lesion or within the surrounding brain tissue as shown by T2 flair or by assuming a circumferential invasion within 1.5–2 cm beyond the enhancing margin [35].

In 2015, the MD Anderson group and Li and colleagues reported that 71% of patients (876 patients) underwent complete excision of all contrast-enhancing tumours. The median survival of the patients was 15.2 months (5.4 months longer than those who underwent subtotal excision).

Their recommendation is that every neurosurgeon should attempt to reset 100% of the contrast-enhancing lesion as this will maximize survival.

They added that the enhancing portion of the tumour is entirely composed of tumour cells with no normal-functioning brain within [43]; then, its excision even when in proximity to the eloquent cortex will not result in extra morbidity.

They also further expanded on the concept that we are currently proposing and attempted to remove T2 flair surrounding the tumour. Overall, 30% of their patients underwent more than 50% T2 flair resection and achieved a survival benefit than those who underwent less than 50% T2 flair resection and fared much better than those who only underwent enhancing tumour excision without T2 Flair resection. The median survival of patients with more than 53.21% T2 resection was 23.2 months, whereas it was 18.7 months in those with less than 53.21% T2 resection in comparison with 15.2 for those who underwent 100% enhancing tumour resection without safety margin [6]; no other study has evaluated such a large number of patients who underwent T2 flair resection.

In our patients, we did not perform neuronavigation, intraoperative CT scans, or MRI; we could not use a similar ‘oedema tracking excision’.

We attempted to excise 100% of what we believed to be the tumour and then removed the remaining surrounding gyri as long as we believed that it would not lead to extra morbidity. In some cases, we took it a step further and performed a complete lobectomy for a GBM within the confines of one lobe.

The best results were found for tumours confined to the temporal lobe with no extra-temporal extensions and anatomical excision of the gyrus or the lobe in which a tumour was involved, with a median survival of 18.45 months. The worst results were found for tumours with extension beyond the confines of the lobe or with extensions through white track fibres or with extensive tumourous oedema, where the median survival was 4 months [Table 5].
Table 5: Six volumetric analysis-based studies

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Our series, although nonvolumetric, follows the same pattern, wherein excision of the safety margin of parenchyma-invading tumour cells leads to a likelihood of delayed disease progression and longer survival.

Patients who underwent more than 100% of tumour excision (anatomical resection) had a mean survival of 16.5 months in comparison with those who underwent GTR, who survived 12.0937 months. The lack of iMRI or CT did not enable a more aggressive excision. We were neither following a radiological image as T2 FLAIR nor we use computerized navigation; instead, we depended on the orientation of the gyral and lobar anatomy and only removed what we believed could be removed safely. The lack of measurable and quantitative and volumetric analysis is a definite limitation of our study, but we can depend only on the available equipment and on the surgeons’ orientation.

The availability of intraoperative navigation makes it easier for surgeons to precisely determine the tumour location, which in turn helps reduce incision and craniotomy size and operative time, and also improves surgical planning and EOR [4],[44],[45].

We hope to repeat this study, but with an intraoperative radiological evaluation of the EOR, RV and amount of nonenhancing glial tissue removed. Postoperative volumetric analysis should also be carried out.

The question now is not whether to perform aggressive resection with a safety margin or not; it is how to achieve this safely and maximally. Relying solely on the surgeons’ experience and operative field orientation is definitely not enough. Orringer et al. [41] documented 69% radiological tumour residual in patients on whom surgeons had performed complete resections.

In many cases, the surgeon might believe that he/she has removed the entire tumour and on follow-up MRI, residual accessible residual may still be there; thus, in the absence of iMRI for detection of EOR, we would advise removal until an anatomical landmark that we know is beyond the extent of the tumour rather than the attempt to differentiate by the naked eye between tumourous tissue and gliotic brain.

The universal concepts of the impact of aggressive resections on outcomes in GBM resulted in the development of new tools that maximize safety and precision including the use of neuronavigation, intraoperative fluorescent dyes and iMRI [46].

iMRI enables visualization of the tumour EOR during surgery and to continue excision of previously thought to be gliosis [47]; iMRI provides extra benefit in 30–40% of all patients in terms of the EOR [48],[49],[50].

We believe that the presence of iMRI is pivotal in safety margin excision whether T2 flair guided or gyral anatomy guided for a circumferential excision of safety margin.

It is advantageous to use 5-aminolevulonic acid, a fluorescein-emitting material that the patient ingests before surgery and is selectively absorbed by the tumour; it is visualized with the operating microscope using special filters. It enables identification of fluorescent tumour tissue in real time within the resection cavity [51], but this advantage is confined to the solid tumour mass but not the infiltrated surrounding brain. Additional benefit is achieved when this is used in conjunction with iMRI in terms of the EOR and residual volume [52].


  Conclusion Top


Total tumour resection with an extra safety margin of tumour-infiltrated gliotic tissue, followed by adjuvant radiochemotherapy results in longer survival than less radical excision. Intraoperative radiological evaluation of EOR will be an essential prerequisite in the near future. All future studies should include detailed volumetric analyses of perioperative radiological evaluations.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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