Original Article
Supratotal Resection: An Emerging Concept of Glioblastoma Multiforme
Surgery—Systematic Review And Meta-Analysis
Peer Asad Aziz1, Salma Farrukh Memon1, Mubarak Hussain1, A. Rauf Memon1, Kiran Abbas2, Shurjeel Uddin Qazi3,
Riaz A.R. Memon1, Kanwal Ali Qambrani1, Osama Taj4, Shamas Ghazanfar3, Aayat Ellahi5, Moiz Ahmed6
- BACKGROUND: The severe neurologic tumor known as
glioblastoma (GBM), also referred to as a grade IV astro-
cytoma, is rapidly progressive and debilitating. Supratotal
resection (SpTR) is an emerging concept within glioma
surgery, which aims to achieve a more extensive resection
of the tumor than is possible with conventional techniques.
- METHODS: We performed a language-independent
search of PubMed, Scopus, and Cochrane CENTRAL to
identify all available literature up to August 2022 of pa-
tients undergoing SpTR assessing survival outcomes in
comparison to other surgical modalities.
- RESULTS: After screening for exclusion, a total of 13
studies, all retrospective in design, were identified and
included in our meta-analysis. SpTR was associated with
significantly increased overall survival (hazard ratio 0.77, 95%
CI 0.71e0.84; P < 0.01, I2 [ 96%) and progression-free survival
(hazard ratio 0.2, 95% CI 0.07e0.56; P [ 0.002, I2 [ 88%).
- CONCLUSION: SpTR is associated with greater overall
survival and PFS when compared with other glioblastoma
surgeries like GTR or SubTR.
INTRODUCTION
G lioblastoma multiforme (GBM) is the most common
malignant primary brain tumor, accounting for approx-
imately 15% of all brain tumors.1 This severe neurologic
Key words
- Astrocytoma
- Glioblastoma
- Supra complete
- Supramarginal resection
- Supratotal resection
Abbreviations and Acronyms
FLAIR: Fluid-attenuated inversion recovery
GBM: Glioblastoma multiforme
GTR: Gross total resection
MRI: Magnetic resonance imaging
PFS: Progression-free survival
PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-analyses
SpTR: Supratotal resection
e46 www.SCIENCEDIRECT.com
tumor, also referred to as a grade IV astrocytoma, is rapidly
progressive and generally fatal. Brain GBMs can form on their
own or grow from lower-grade astrocytoma. Although it colo-
nizes the nearby brain tissue, it generally does not metastasize to
other organs.2 The main form of treatment for this type of glioma
is surgical resection or excision, which is subsequently
complemented by adjuvant radiation and chemotherapy.2
Supratotal resection (SpTR) is an emerging concept within
GBM surgery, which aims to achieve a more extensive resection of
the tumor than is possible with conventional techniques.3 This
technique involves the removal of more than 100% of the visible
tumor tissue, which means that the surgeon removes not only
the tumor itself but also some surrounding healthy brain tissue.3,4
True SpTR is defined as excision past all discernible and visible
magnetic resonance imaging (MRI) abnormalities, including fluid-
attenuated inversion recovery (FLAIR) borders. This may be
accomplished with 5-ALA-guided tumor tissue elimination, using
intraoperative MRI for non-enhancing residual tumors, or resec-
tion until improvement in clinical outcome is achieved.5 SpTR is
therefore more extensive than gross total resection (GTR), which
involves removal of the visible tumor only.6,7 This raises the
probability of progression-free recession and, eventually, sur-
vival, while lowering the likelihood of recurrence. The procedure
has been shown to be safe and effective in multiple studies, and its
use is increasing in clinical practice.6,7
In a meta-analysis of glioblastoma patients, Brown et al. found a
correlation between the size of the resection and survival.8 Patients
who had more tissue removed after surgery did better than those
who had less extensive resections, according to a study of 37
studies. These findings suggest that maximal safe surgical
resection should be considered in the treatment of glioblastoma.
From the 1Department of Neurosurgery, Liaquat University of Medical Health Sciences,
Jamshoro, Pakistan; 2Department of Community Health Sciences, Aga Khan University,
Karachi, Pakistan; 3Department of Internal Medicine, Dow University of Health Sciences,
Karachi, Pakistan; 4Department of Internal Medicine, Creek General Hospital, Karachi,
Pakistan; 5Department of Internal Medicine, Jinnah Sindh Medical University, Karachi,
Pakistan; and 6Department of Cardiology, National Institute of Cardiovascular Diseases,
Karachi, Pakistan
To whom correspondence should be addressed: Peer Asad Aziz, M.B.B.S.
[E-mail: azizpirasad@gmail.com]
Citation: World Neurosurg. (2023) 179:e46-e55.
https://doi.org/10.1016/j.wneu.2023.07.020
Journal homepage: www.journals.elsevier.com/world-neurosurgery
Available online: www.sciencedirect.com
1878-8750/$ - see front matter ª 2023 Published by Elsevier Inc.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2023.07.020

PEER ASAD AZIZ ET AL.
However, SpTR is not without its challenges.9 The procedure
requires a high degree of technical expertise and specialized
equipment, which may not be available at all medical centers.
Additionally, the procedure carries a higher risk of surgical
complications such as neurologic deficits, which can have a
significant impact on patient outcomes.9 Several studies suggest
that the potential benefits of SpTR could be insignificant and
that other factors, such as the patient’s age, general health, and
the location and size of the tumor might be more important
survival predictors.9,10
The decision to perform SpTR should generally be based on a
thorough evaluation of the patient’s particular circumstances,
including the risks and advantages of the treatment, as well as the
patient’s overall wellbeing and expectations. This decision should
be made in consultation with a team of medical professionals,
including neurosurgeons, oncologists, and other specialists, who
can provide the best possible care for the patient.9,10
This meta-analysis was performed to determine patient survival
rates and progression-free survival rates of glioblastoma patients
who underwent SpTR.
METHODS
Protocol and Registration
We adhered to the established standards of the Preferred
Reporting Items for Systematic Reviews and Meta-analyses
(PRISMA) to correctly report this systematic review and meta-
analysis.11 The protocol has been tentatively registered and
published in PROSPERO (www.crd.york.ac.uk/PROSPERO, CRD
42022366204).
Search Strategy
Six databases, including PubMed, EMBASE, The Cochrane Li-
brary, Web of Science, Scopus, and ClinicalTrials.gov, were
thoroughly searched for relevant literature from their inception
through August 20, 2022. The following search string was utilized
to obtain pertinent articles: (supra total resection OR glioma
resection OR supra marginal OR supra complete) AND (glioma
OR glioblastoma OR GBM OR glioblastoma multiforme OR as-
trocytoma OR ependymoma OR oligodendroma) AND (resections
OR margin resections OR tumor-free margins OR FLAIR region).
Furthermore, the reference lists of the retrieved trials, meta-
analyses, research papers, and review articles were manually
browsed to identify any published literature on this topic.
Study Selection
All the studies included in this meta-analysis satisfied the
following eligibility criteria: (a) published case-control or pro-
spective/retrospective cohort studies; (b) patients who were diag-
nosed with GBM; (c) glioblastoma patients who underwent SpTR;
(d) supratotal GTR total resection.
SpTR was defined as complete resection of contrast-enhanced
region of the tumor with additional resection of different per-
centages of FLAIR region.
WORLD NEUROSURGERY 179: e46-e55, NOVEMBER 2023
ORIGINAL ARTICLE
GLIOBLASTOMA MULTIFORME SURGERY
Data Extraction and Quality Assessment
The output of the systematic search was exported to the EndNote
Reference Library program and any duplicate entries were elimi-
nated. Two independent reviewers (S.U.Q. and M.A.) thoroughly
assessed all the articles and only the trials that satisfied the pre-
determined criteria were included. A third investigator (K.A.)
rectified any discrepancies. The initial author’s name, the year of
publication, the study’s location, its design, its sampling pro-
cedures, the number of patients who received SpTR, and the
number of patients handled with other surgical techniques were
all extracted from the trials. The overall survival of SpTR was the
main endpoint of interest. The secondary outcomes of interest
were surgical risk of complications and focal impairments. Two
separate researchers evaluated the caliber of the qualifying studies
using an observational variation of the Newcastle-Ottawa Scale.
Any disputes were resolved via dialogue and effective
communication.
Statistical Analysis
Review Manager (version 5.3; The Nordic Cochrane Centre, The
Cochrane Collaboration, 2014, Copenhagen, Denmark) was used
to conduct the statistical evaluation. A general inverse variance
function was used to aggregate the overall survival hazard ratios
and the 95% CIs, which was then assessed using a random effects
model. For continuous outcomes, mean differences along with
their standard deviations were meta-analyzed using the random
effects model. We analyzed statistical heterogeneity using
Cochrane Q and I2 statistics.12 The Egger asymmetry test and a
visual inspection of the funnel plot were used to assess the
publication bias. A P-value of <0.05 was regarded as significant
in all cases.
RESULTS
Literature Review
The process for choosing and searching for studies is outlined in
the PRISMA chart (Figure 1). The initial search produced 13,300
results. A total of 1,744 articles were selected for screening and
were approved. We excluded 750 papers because they did not
include patients with SpTR, as well as 136 studies where the
variable of interest was not mentioned. Two articles written in
other languages were not included. We considered a total of 13
papers in our meta-analysis.12-24
Study Characteristics
All of the studies were retrospective in design. A total of 20,726
patients were included in the analysis, with a male-dominant
patient population (n ¼ 11,820, 57%). The age in our population
ranged from 38 to 63 years. In our sample, 212 individuals un-
derwent SpTR, 473 underwent GTR, 300 underwent subtotal
resection, and 165 underwent partial resection. The baseline
characteristics of the included studies and their individuals are
compiled in Table 1.
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PEER ASAD AZIZ ET AL. GLIOBLASTOMA MULTIFORME SURGERY

Records removed before

Identification
Records identified from:
screening:
Databases (n =6)
Duplicate records
Registers (n = 13,300)
removed (n =5,500)

Records screened Records excluded

(n =7,800) (n =5,867)
Screening

Reports sought for retrieval Reports not retrieved

(n =1,933) (n =200)

Reports excluded:
Reports assessed for Reviews (n =810)
eligibility (n =1,744) Studies that did not meet
inclusion criteria (n =750)
Outcomes not reported (n
=136)
Study not in English (n=2)
Studies included for
qualitative synthesis (n=35)
Included

Studies included in
quantitative synthesis
(n= 13)

Figure 1. PRISMA chart summarizing the literature search.

Overall Survival with SpTR
All studies reported overall survival with SpTR. SpTR was asso-
ciated with a significant increase in overall survival (hazard ratio
[HR] 0.78, 95% CI 0.72e0.85; P < 0.01, I2 ¼ 96%). A high het-
erogeneity was observed, as shown in Figure 2.
Progression-Free Survival with SpTR
Four studies reported progression-free survival (PFS). SpTR was
associated with a significantly increased PFS (HR 0.2, 95% CI
0.07e0.56; P ¼ 0.002, I2 ¼ 88%), as shown in Figure 3. In
addition, we observed that duration of PFS was significantly
increased with SpTR as compared with other surgical subtypes
(Figure 4).
Assessment of Heterogeneity
The assessment of study quality revealed that the included studies
had scores in the medium range and a high risk of bias.
(Supplementary Table 1). Among them, 3 studies did not select
patients who were true representatives of the cohort.15,22,23 All
studies matched the experimental and control groups based on

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PEER ASAD AZIZ ET AL.

Table 1. Baseline Characteristics of Included Studies
Population, n (%) Tumor Location IDH 1 Status, n (%) Surgery Type, n (%)

Age Mean  SD, Insular/ Wild

No. Study yeaers Male Female Frontal Parietal Occipital Temporal Deep Type Mutation Supratotal GTR Partial Subtotal

1 Motomura et al.13 42.8 74 (58.7%) 52 (41.3%) 73 (57.9%) 12 (9.5%) 1 (0.8%) 13 (10.3%) 27 (21.4%) 21 105 15 (11.9%) 32 (25.4%) 52 27 (21.4%)
(16.7%) (83.3%) (41.3%)
2 Vivas-Buitrago 59.8  17 68 (67%) 34 (33%) 47 (46.5%) 26 14 46 (45.5%) 51 (50.5%)
et al.12 (25.7%) (13.9%)
3 Rossi et al.15 38.9  11.8 195 (61.1%) 124 (38.9%) 188 59 71 (17.6%) 86 (21.3%) 37 (9.2%) 367 127 (31.4%) 166 (41.1%) 96 15 (3.7%)
(46.5%) (14.6%) (90.8%) (23.7%)
4 Moiraghi et al.14 63  12.6 251 (55.4%) 202 (44.6%) 170 89 17 (3.8%) 137 21 (4.6%) 16 (3.5%) 150 (33.1%) 98
(37.5%) (19.7%) (30.2%) (21.6%)
5 Rho et al.24 48  16 64 (56.6%) 49 (43.4%) 70 (61.9%) 33 (29.2%) 62 18 (22.5%)
(77.5%)
Mampre et al.16 59.9  13.48
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6 149 (61%) 96 (39%) 11 (5%) 84 (34%) 161 (66%)

7 Liu et al.20 55.7  18.8 758 (62%) 471 (38%)
8 Eyupogolu et al.22 53  16 60 (57.1%) 45 (42.9%)
9 Glenn et al.18
54.9  14.6 25 (78.1%) 7 (21.9%) 21 3 (9.4%) 7 (21.9%) 9 (28.1%) 16 (50%)
(65.6%)
Esquenaizi et al.19 56  15

GLIOBLASTOMA MULTIFORME SURGERY

10 57 (66%) 29 (34%) 28 (33%) 19 (22%) 36 (42%) 3 (3%)
11 De Bonis et al.17 57.5  14.7 47 (53.4%) 41 (46.6%) 36 (40.9%) 52 (59.1%)
12 Hamada et al. 21
48.57  15.3 43 (73%) 16 (27%) 4 (24%) 12 (55%) 4 (51%)
13 Rivera et al.23 73  2.5 9581 7782 2907 2451 4879
(55.8%) (44.2%) (16.5%) (13.9%) (27.6%)

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Figure 2. Overall survival with SpTR.

baseline demographics and the presence of glioblastoma;
however, only 4 studies reported the IDH1 mutation status of
GBM. Four studies used record linkage to determine
outcomes.15,16,22,23
Publication Bias
Publication bias was assessed by visual inspection of funnel plots.
We observed a high asymmetry in the outcome PFS
(Supplementary Figure 1). Moderate level asymmetry was observed
with overall survival benefit of SpTR (Supplementary Figure 2).
DISCUSSION
Our meta-analysis revealed that SpTR was associated with a sig-
nificant improvement in overall survival when compared with
other surgical techniques. Other resection subtypes were associ-
ated with a significantly decreased PFS as compared with SpTR.
A few studies have reported varying findings on the effective-
ness of SpTR in glioblastoma, with some suggesting that the
procedure can lead to improved survival rates and others sug-
gesting that the benefits may be limited. It is important to note
that the decision to pursue SpTR should be made on an individual
basis, considering a range of patient- and tumor-specific factors,
and being overseen by a group of medical experts with expertise in
the field.24-28
SpTR in glioblastoma was the subject of a thorough literature
review in the 2019 Neuro-oncology paper by de Leeuw and Vogel-
baum.29 The authors set out to summarize the benefits and
drawbacks of performing glioma surgery with less than
complete removal of the projected tumor volume. The authors
determined that 11 trials, totaling 548 patients, satisfied their
inclusion requirements. The studies were all retrospective and
included both high- and low-grade gliomas. The majority of
studies relied on intraoperative imaging methods like MRI to
gauge the extent of resection.

Figure 3. Progression-free survival with SpTR.

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PEER ASAD AZIZ ET AL.
Figure 4. Duration of progression-free survival with SpTR.
The main finding of the review was that SpTR of gliomas is
related with improved overall survival and progression-free sur-
vival when compared with subtotal resection. Similar results were
also seen when SpTR was compared with subtotal resection. The
main difference between the 2 types of resections is that the
subtotal resection removes all the tumors, while the partial
resection removes only the major tumors. Although the extent of
resection varied between studies, some reported a maximum
extent of resection of 110% and others reported up to 160% of the
predicted tumor volume being removed. The researchers also
noted that SpTR was associated with a higher likelihood of
neurologic impairments and postoperative problems, such wound
infections.29
We found that different aspects of the disease were studied in
affiliated literature on the subject, and provided distinct insights on
how to potentially navigate therapeutic intervention. The effects of
supramarginal resection on survival outcomes following GTR of
IDH-wild-type glioblastoma, for instance, were investigated in the
study by Vivas-Buitrago et al.12 The study looked at 219 people who
underwent surgery for IDH-wild-type glioblastoma, and it found a
correlation between supramarginal resection and longer overall
survival and PFS. The investigators’ conclusion is that supra-
marginal resection may improve survival outcomes for individuals
with IDH-wild-type glioblastoma. On the other hand, the study by
Anselmo et al.30 aimed to clinically characterize glioblastoma
patients living longer than 2 years. The study analyzed the
medical records of 68 patients from 2 Italian institutions who
survived for more than 2 years after the initial diagnosis of
glioblastoma. The authors found that patients who survived for
longer than 2 years were more likely to be younger, have a lower
Karnofsky Performance Status score, and receive a combination of
temozolomide and radiotherapy as the initial treatment.
Additionally, patients who underwent a second surgery for
disease progression had a longer survival than those who did not.
WORLD NEUROSURGERY 179: e46-e55, NOVEMBER 2023
ORIGINAL ARTICLE
GLIOBLASTOMA MULTIFORME SURGERY
While both studies provide insights into glioblastoma survival
outcomes, they focus on different aspects of the disease. Vivas-
Buitrago et al. emphasize the importance of surgical technique
and suggest that supramarginal resection could improve survival
outcomes in IDH-wild-type glioblastoma patients.12 Anselmo et al.
characterize the clinical features of glioblastoma patients who
survived for more than 2 years and highlight the potential
benefits of a combined treatment approach and re-surgery for
disease progression.30
The thorough 2021 study by Motomura et al.13 used awake brain
imaging to analyze the impact of resection size on survival in
patients with grade II and grade III gliomas. The study included
57 patients who underwent SpTR, which was defined as
resection of more than 100% of the estimated tumor volume.
The extent of resection was found to be a significant predictor
of overall survival by the researchers, with patients receiving
SpTR living longer overall than those receiving partial resection.
In addition, the study found that awake brain mapping was safe
and effective for identifying functional areas and achieving
SpTR. The researchers postulated that SpTR using awake brain
mapping may be an advantageous surgical technique for
improving the prognosis for survival with grade II and grade III
gliomas.13
The surgical approach and its impact on survival outcomes for
patients with different types of gliomas are described in the
studies by Moiraghi et al.14 and Rossi et al.15 The possibility,
effectiveness, and effect on overall survival of awake resection in
patients with recently diagnosed supratentorial IDH-wild-type
glioblastomas were examined by Moiraghi et al. in 2021. The
study found that awake surgery was feasible and safe, with a low
rate of complications, and suggested that it could be a valid option
for selected patients.
In contrast, the Rossi et al. (2021) study investigated the rela-
tionship between SpTR and survival from lower-grade gliomas,
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PEER ASAD AZIZ ET AL. GLIOBLASTOMA MULTIFORME SURGERY

survival without progression, malignant transformation, and
overall survival.15 SpTR was connected to better overall survival
rates, including PFS and overall survival, after surgery for 341
individuals with low-grade gliomas, but it had no impact on
how quickly tumors developed into malignancies.
Overall, both studies highlight the importance of surgical
technique in improving survival outcomes in patients with gli-
omas. However, they focus on different types of gliomas and
different surgical approaches. Lower-grade glioma patients who
receive SpTR may have a better chance of surviving. Nevertheless,
as demonstrated by Moiraghi et al., awake surgery may be a
possibility for some patients with IDH-wild-type glioblastomas.14
Using selective cortical mapping and the subpial technique,
Esquenazi et al. assessed the effect of supratotal resection on the
survival of glioblastoma patients.19 The scientists conducted a
retrospective study of 103 patients who underwent surgery for
glioblastoma and found that those who underwent SpTR had a
significantly longer median overall survival time than those who
underwent less severe resection. The experts found that patients
who received SpTR had a lower risk of tumor recurrence than
those who received less extensive resection. According to the
study’s findings, glioblastoma patients may have a selective
advantage when undergoing SpTR using the subpial technique
and selective cortical mapping.
The results and findings of our review should be interpreted
with caution due to its limitations. The included studies in our
meta-analysis were underpowered, which could have introduced
biases in the results. A particular location of GBM was not
resected and compared across studies, which could have impacted
the survival of patients. There was under-representation of female
patients in the cohorts, which may have led to gender disparity in
the results. In addition, the studies did not compare the outcomes
of SpTR with each individual surgery subtype due to which it may
have overestimated or underestimated the results.
CONCLUSIONS
In conclusion, we found that SpTR is associated with greater
overall survival and PFS when compared with other glioblastoma
surgeries like GTR or SubTR. The present study suggests that
SpTR can be a useful strategy for improving outcomes in glioma
surgery, but it should be balanced against potential risks and in-
dividual patient factors. Further research is required to determine
the benefits and downsides of this treatment and to specify the
ideal level of resection for the different subtypes of glioma. The
present study underscores the complex and multifaceted nature of
glioblastoma and the need for a personalized and multidisci-
plinary approach to treatment.
CRediT AUTHORSHIP CONTRIBUTION STATEMENT
Peer Asad Aziz: Conceptualization, Supervision, Methodology.
Salma Farrukh Memon: Conceptualization, Supervision, Meth-
odology. Mubarak Hussain: Writing e review & editing. A. Rauf
Memon: Writing e review & editing. Kiran Abbas: Resources,
Data curation, Project administration. Shurjeel Uddin Qazi:
Writing e original draft, Data curation. Riaz A.R. Memon:
Writing e original draft, Data curation. Kanwal Ali Qambrani:
Writing e original draft, Data curation. Osama Taj: Writing e
original draft, Data curation. Shamas Ghazanfar: Writing e review
& editing, Formal analysis, Resources, Investigation. Aayat Ellahi:
Formal analysis, Resources, Investigation. Moiz Ahmed:
Writing e review & editing, Visualization.

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 SUPPLEMENTARY DATA
e54

PEER ASAD AZIZ ET AL.

www.SCIENCEDIRECT.com

Supplementary Table 1. Quality Assessment of Included Studies Using Newcastle Ottawa Scale
Selection Comparability Outcome

Study/Score S1 S2 S3 S4 C O1 O2 O3 Total
12
Vivas-Buitrago et al., 2020 * * * * * * * 7
17
De Bonis et al., 2013 * * * * * * 5
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2023.07.020

19
Esquenazi et al., 2017 * * * * * * * 6
Eyupogolu et al., 201622 * * * * * * * 5
Glen et al., 201818 * * * * * * * 7
Hamada et al., 201321 * * * * * * * * 5
24
Rho et al., 2019 * * * * * * * 6
20
Liu et al., 2016 * * * * * * * 7
Mampre et al., 201816 * * * * * * * 7
13
Motomura et al., 2021 * * * * * * * 7
Rivera et al., 202123 * * * * * * * 5
Rossi et al., 202115 * * * * * * * 5

GLIOBLASTOMA MULTIFORME SURGERY

The symbol ‘*’ means that the study met the relevant criteria of the quality assessment of Newcastle-Ottawa Scale.

ORIGINAL ARTICLE
 ORIGINAL ARTICLE
PEER ASAD AZIZ ET AL. GLIOBLASTOMA MULTIFORME SURGERY

Supplementary Figure 1. Funnel plot for progression-free survival with

SpTR.

Supplementary Figure 2. Funnel plot for overall survival with SpTR.

WORLD NEUROSURGERY 179: e46-e55, NOVEMBER 2023 www.journals.elsevier.com/world-neurosurgery e55