PERITUMORAL BRAIN EDEMA IN MENINGIOMAS: CORRELATION WITH

SURGICAL FINDING AND PROGNOSIS

Alaa A. Farag, Ahmed M. Seleem

Faculty of Medicine, Banha University

Abstract

Backgound: Peritumoral brain edema (PTBE) in meningiomas had been a subject of interest;

its occurrence in an extraaxial tumor was the reason of many studies and published data.

Objective: The goal of this study was to evaluate and to determine the exact implication of

Peritumoral brain edema in meningiomas in intraoperative and short postoperative prognosis.

Subjects and Methods: During 2006 to 2011, 45 patients with supratentorial meningiomas

were studied. Intraoperatively certain findings were reported including: easy or difficult

resection, simpson’s grade of removal, brain tumor interface, plane of cleavage, pial

vascularization of the tumor and arachnoid disruption. Morbidity and mortality were

recorded; also postoperative CT and/or MRI were obtained within the first 3 months.

Results: There were 26 meningiomas (57.7%) with peritumoral edema and 19 meningiomas

without (42.3%). Pial vascularization of the tumor was defined in 24 patients (53.3%), 4

patients (21%) had a pial blood supply in edema negative group compared to 20 patients

(76.9%) in edema positive group. In this study, there was 1 case mortality (2.2%) in edema

positive group. As regard morbidity, 8 (30.6%) patients in edema positive group suffered an

early postoperative morbidity this is in comparison to 4 patients (21%) in the edema negative

group. Conclusion: Our study shows that PTBE in meningiomas affects the surgical

prognosis and confers a higher risk of morbidity and postoperative complications.

Preoperative management of PTBE and immediate post-operative monitoring are important.

Key words: Meningioma, Brain edema

Corresponding Author: Alaa A. Farag, Alaa A. Farag, Assistant Professor of Neurosurgery,

Faculty of Medicine, Banha University. email: alaa1farag@yahoo.com

Introduction

Meningioma possesses the ability to produce peritumoral brain edemas (PTBE) despite

its extracerebral origin and being a benign and a slow-growing tumor.1,2

Peritumoral edema is

present in at least half of the cases of meningioma, and it may be present in varying degrees

and in an unpredictable fashion.3

Unlike intraaxial tumors, whose physiopathology is attributed to hematoencephalic

barrier disorder, the precise mechanism of peritumoral edemas is still unknown.4 Different

theories have been proposed to explain its formation: mechanical factors such as tumoral

compression to the adjacent parenchyma causing cerebral ischemia5,6

or the compression of

large veins and/or sinus vein that produce vein stasis6. The secretor-excretory phenomenon

with the production of edemagen substances7,8

, as well as hydrodynamic factors that produce

breakage of the hematoencephalic barrier are studied hypothesis.9,6

More recently, Tanaka

and Colleagues10

proposed that PTBE could be related to the tumor drainage vein hypoplasia.

For some authors, management is more difficult if meningiomas are associated with

PTBE11

, but this is controversial.12

Overall, little is known of prognostic factors Influencing

morbidity and mortality after intracranial meningioma surgery13

.

Aim of the work: The goal was to evaluate and to determine the exact implication of

peritumoral brain edema in benign meningiomas in intraoperative and short postoperative

prognosis.

Subjects and Methods

During 2006 to 2011, 45 patients with benign supratentorial meningiomas were

studied. Clinical the duration of clinical

The clinical variables considered were the age and sex of the patient, the duration of

clinical history (months), and the existence of focal deficits, seizures (focal or generalized), a

psychorganic syndrome (including decreased level of consciousness), and an intracranial

hypertension syndrome.

All patients underwent MRI before surgery. The size of the tumor was calculated by

multiplying the maximum coronal, axial anteroposterior and axial mediolateral tumor

diameters on MRI. The area of PTBE, including the tumor, was obtained using the same

method. Edema Index (EI) was calculated by dividing the size of the PTBE by that of tumor,

thus, if EI = 1, there is no PTBE.

Figure 1: T2 MRI Shows the lesion without oedma around.

The edema was identified as either a hyperintense image in MRI in T2-weighted

scans or hypointense in T1 weighted scans. Presence and absence of calcifications was also

evaluated.

Figure 2: T2 MRI Shows the lesion with oedma around.

Perioperative care, each case included in this study was given IV antibiotics (third

generation cephalosporin in most cases) 1 hour before surgery, and continued during the

operation as needed, and for 48 hours after surgery or until all drains and long lines were

removed. Steroids ―dexamethazone‖ was given as needed in cases with vasogenic edema and

was started at least 48 hours before surgery, continued during surgery, and gradually tapered

over 4-5 days following surgery. All the cases were operated upon by the staff members in

the neurosurgical department.

Microscopic removal of the tumor was done whenever possible and whenever needed.

Intraoperatively certain finding were reported including; easy or difficult resection, simpson’s

grade of removal, brain tumor interface, plane of cleavage, pial vascularization of the tumor

and arachnoid disruption.

Histopathological examination of tumor specimen were done and reported. Morbidity

and mortality were recorded; also postoperative CT and/or MRI were obtained within the first

3 months and were evaluated for presence of tumor residue, resolution of edema, and

secondary effect on brain parenchyma.

Statistical Analysis: Continuous data are presented as mean and standard deviation.

Dichotomous or categorical data are presented as number and percent. Comparison between

patients with peritumoral brain edema and patients without edema regarding categorical or

dichotomous variables was done by using Chi square test or Fischer exact test. Level of

significance was considered at P value ≤ 0.05. SPSS 19 was used for statistical analysis.

Results

Data of this study was collected from 45 cases of supratentorial intracranial benign

meningiomas were analyzed and the results were evaluated. The study included 45 patients

30 females and 15 males whose age ranged between 29 and 69 years, mean age was 51.7

years ± 1.6. In this study headache was the prevalent symptom in the course of illness, 40

patients (88%) was presenting with headache. In this study, 20 patients (44.5%) presented

with seizures in the course of illness. In this study, there were 26 meningiomas (57.7%) with

peritumoral edema (Figure 2) and 19 meningiomas without edema (42.3%) (Figure 1).

According to location; tumors were classified into convexity, olfactory groove, falcine,

parasagittal, sphenoid wing, tuberculum sella, and suprasellar; table 1. In this study, sphenoid

wing, falcine and olfactory groove meningiomas have the highest mean edema indices 3.48,

3.14, and 2.64 respectively.

Table 1: Comparison between edema (-) and edema (+) as regards location

Edema (-) Edema (+) Total

n % n % n %

Convexity 10 52.6% 13 50% 23 51.0%

Falcine 0 0% 3 11.5% 3 6.6%

Olfactory

groove

0 0% 4 15.4% 4 8.8%

Parasagittal 5 26.3% 3 11.5% 8 17.7%

Sphenoid wing 2 10.5% 3 11.5% 5 11.1%

Suprasellar 1 5.2% 0 0% 1 2.2%

Tuberculum

sella

1 5.2% 0 0% 1 2.2%

Total 19 100.0% 26 100.0% 45 100.0%

n: Number of patient, %: Percent

All cases had underwent surgical removal, and certain intraoperative factors were

recorded and analyzed; Simpson grade of removal, brain tumor interface, crossing pial blood

vessel to the tumor, and surgical plane of cleavage; table 2.

Twenty patients (44.5%) excised with Simpson grade 1, 18 patients (40%) with grade

2, and 7 (15.5%) with grade 4 removal. There was no correlation between degree of removal

and incidence of edema.

Intraoperative brain tumor interface was defined in 31 patients (68.8%), 16 patients

(84.2%) had a defined brain tumor interface in edema negative group compared to 15 patients

(57.6%) in edema positive group (P = 0.06).

Intraoperative surgical plane of cleavage was defined in 30 patients (66.7%), 16

patients (84.2%) had a defined surgical plane of cleavage in edema negative group compared

to 14 patients (53.8%) in edema positive group (P = 0.03). Surgical plane of cleavage

correlated to the severity of peritumoral edema.

There was a very strong association between incidence of peritumoral edema and

presence of pial blood supply. Pial vascularization of the tumor was defined in 24 patients

(53.3%), 4 patients (21%) had a pial blood supply in edema negative group compared to 20

patients (76.9%) in edema positive group (P < 0.001).

Table (2): Comparison between edema (-) and edema (+) as regards intra-operative finding

Edema (-) Edema (+) Total

n % n % n %

Simpson grade G1 9 47.3% 11 42.3.4% 20 44.4%

G2 7 36.8% 11 42.3% 18 40.0%

G4 3 15.7% 4 15.3% 7 15.6%

Total 19 100.0% 26 100.0% 45 100.0%

Defined brain

tumor interface

No 3 15.8% 11 42.4% 14 31.1%

Yes 16 84.2% 15 57.6% 31 68.9%

Total 19 100.0% 26 100.0% 45 100.0%

Complete plane

of cleavage

No 3 15.8% 12 46.2% 15 33.4%

Yes 16 84.2% 14 53.8% 30 66.6%

Total 19 100.0% 26 100.0% 45 100.0%

Pial supply No 15 79.0% 6 23.1% 21 46.7%

Yes 4 21.0% 20 76.9% 24 53.3%

Total 19 100.0% 26 100.0% 45 100.0%

n: Number of patient, %: Percent, G: grade

Postoperatively patients were followed during the first three months, in concern with

mortality, and morbidity.

In this study, there was 1 case mortality (2.2%) that died early during follow-up, in the

edema positive group, death was related to intraoperative procedure during excision that was

followed by extensive infarction and edema.

As regard morbidity, 8 patients (30.6%) in edema positive group suffered an early

postoperative morbidity ranging from controlled fits to deep coma; this is in comparison to 4

patients (21%) in the edema negative group.

Discussion

Despite primarily extraaxial locations, slow progression rates, and usually benign

histologic characteristics, meningiomas are frequently associated with PTBE.3 Peritumoral

brain edema is found in approximately 50% of meningiomas.14

Clinically, perioperative

mortality and morbidity in menigioma surgery may be attributed to PTBE in meningioma.

Hence, significant brain edema may cause severe neurologic deficits and limit the surgical

field during the approach.3

Meningiomas are separated from the white matter by the arachnoid membrane, the

subarachnoid space, the pia mater, and the cerebral cortex that are formed from a dense

network of neuronal and glial processes resistant to the fluid flow.5 The arachnoid is

impervious to fluid, and pia mater is less permeable to edema protein.7 Despite of that

resistance, approximately 60% of meningiomas are associated with peritumoral brain

edema.4,6,15

In this study, we evaluated the surgical finding and prognosis of PTBE in

meningiomas. The majority of our patients (57.7%) had PTBE on preoperative imaging, in

agreement with previous findings.12

The incidence of PTBE was 57.7% in our patient

population and ranges from 45% to 92% in other reports.16-18

At present, there are no unanimous results regarding tumoral location. Most cited the

following locations having a higher connection with a larger edema incidence; convexity6,9,19

,

parasagittal9,19

, falx6, sphenoidal wing

20, frontobasal

15,19,20, and medium fossa.

15 Other

authors mention a lower edema incidence among tumors located at the posterior fossa6,19

and

tentorium6 may be because these exhibit symptoms more precociously or due to a smaller

amount of white matter at the posterior fossa. In this study, sphenoid wing, falcine and

olfactory groove meningiomas have the highest mean edema indices 3.48, 3.14, and 2.64

respectively.

When surgical findings were evaluated, Salpietro and Colleages2 verified the

existence of relationship between invasive tumors and edema extension. A study published

by Tamiya and Colleages21

in 2001 analyzed 175 cases, indicating as predictive factors

peritumoral edema, disappearance of tumor-brain arachnoid layer interface visible in T2 by

nuclear magnetic resonance, and tumor pial vascularization pattern.

In our opinion, the easier the surgical plane is to detect, the easier the resection. On

the other hand, when resection is difficult, the brain/meningioma interface is not clearly

identifiable. We found Intraoperatively surgical plane of cleavage was defined in 30 patients

(66.7%), 16 patients (84.2%) had a defined surgical plane of cleavage in edema negative

group compared to 14 patients (53.8%) in edema positive group. Surgical plane of cleavage

correlated to the severity of peritumoral edema.

The pial-cortical arterial supply of meningiomas reflects the close spatial relationship

between the tumor surface and the adjacent brain parenchyma. The arachnoid, which serves

as a physiological barrier between the brain and extraaxial structures such as the meningioma,

is either penetrated by the cerebral vessels or infiltrated by the tumor.4 A recently published

study demonstrated a strong correlation between the pial-cortical blood supply and the

occurrence of edema, in agreement with our results.3 In our study There was a very strong

correlation between incidence of peritumoral edema and presence of pial blood supply. Pial

vascularization of the tumor was defined in 24 patients (53.3%), 4 patients (21%) had a pial

blood supply in edema negative group compared to 20 patients (76.9%) in edema positive

group.

Overall mortality of meningioma surgery is variable in the literature, ranging from 2%

to 23%.12,22

In this study, there was 1 case mortality (2.2%) that died early during follow-up,

in the edema positive group, death was related to intraoperative troubles during excision that

was followed by extensive infarction and edema.

Edema was related to higher morbidity in the surgical management of meningiomas.

For example, PTBE was associated with a longer hospital stay, increased difficulty of

surgical resection, and increased risk of postoperative intracranial hematoma and intracranial

hypertension compared to meningiomas without PTBE12

.

In our study, morbidity was 8 (30.6%) patients in edema positive group suffered an

early postoperative morbidity ranging from controlled fits to deep coma; this is in comparison

to 4 patients (21%) in the edema negative group.

Conclusion

Our study shows that PTBE in meningiomas affects the surgical prognosis and

confers a higher risk of morbidity and postoperative complications. Preoperative management

of PTBE and immediate post-operative monitoring are important.

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الملخص العربى

العالقة مب بين الوذمة المخية المصبحبة للورم السحبئى واالستئصبل الجراحي وحبلة المريض بعد إجراء الجراحة

انغسض ي ر اندزاسج دقييى أثس انذيج انخيج انصبحتج نهزو انسحبئ عه يجسيبح األيز أثبء األسذئصبل

انجساحىى لىىرنى عهىى حبنىىج انىىسيط ة ىىد انجساحىىج يتبعىىسث ليليىىج انذ بيىىم يىىو انىىزو ىى ىى ىىر انذيىىج أثىىبء ة ىىد

انزو انخ انسحبئ .انجساحج يتبعسث نذال انعبعلبح انصبحتج ألسذئصبل

يسيعب ي انصبةي ةبنزو انسحبئ يسذشل ةب انجبي ى انلذىسث يىب 54قد أ سيخ ر اندزاسج عه

يو إعذتبز لم انشاد اإللهييكيج انلحصبح عم أع ج ةبنسي انغبغيس عهى انى 6022إن عبو 6002ةي عبو

انشاد أثىبء انجساحىج انصى ةبح أثىبء األسذئصىبل انجساحى حىد إسذئصىبل انىزو يو دسجيم زصد لم ان اليبح

ي بيم سس( انحد انلبصم يىب ةىي انىزو انى األعيىج اندييىج ان ىبةسث يى األو انحى إنى انىزو لىرنى دسىجيم

نىسيط عىىم أعى ج يق يىج زىىي األثىبز انسىهتيج انذسدتىج عهىى انجساحىج حىبيح ان يىىبح لىرنى عى غسيىى يذبة ىج ا

يغبغيس عه ان خالل انشز انثالر األنى يىو دقيىيى ى ةقبيىب يى انىزو يى عديى يىد عىحي انذيىج انخيىج

لرنى األثس انسهت عه ان ساء ر انذيج .

ي انسبء 00يسيعب يى 54قد دى و لم ر انتيببح دحهيهب دقييى انذبئج قد أعذهخ ر اندزاسج عه

عبيب قد ةهى عىد يى ي ىب يى انذيىج انخيىج انصىبحتج نهىزو 22إن 62ي انس بل لب ي دل انس يب ةي 24

( ي ي ىىد ةىىى انذيىىج انخيىىج 56.0يسيعىىب ةسىىتج % 22( 26.6 % يسيعىىب ةسىىتج 62انسىىحبئ ىى ىىر اندزاسىىج

( ة بيىم سسى يى اندز ىج األنى 55.4يسيعىب ةسىتج % 60انصبحتج نهزو انسحبئ قد دىى إسذئصىبل انىزو ى

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اندز ج انساة ج .( ة بيم سس ي24.4 %

%( يى انجعىج انذى د ىب يى انذيىج انخيىج 6.6 ر اندزاسج لبىخ ىبح حبنىج ىبث احىدث ةسىتج

( يى انجعىج 62يسظى %5( يقبزىج ة ىد 00.2يسظ عب يى يعىبعلبح يىب ة ىد انجساحىج % 1انصبحتج (

انذ ي د ب ي انذيج انخيج .

زاسج ة د يقبزذب ةب شس ى اندزاسىبح انشىبةج أ انذيىج انخيىج انصىبحتج نهىزو انسىحبئ قد خهصخ اند

دؤثس عه حبنج انسيط أثبء انجساحج ة دب لرنى ألدح اندزاسج أ انذيج انخيج عبيم ي عايم انخ س انذ دؤ

ب قتم انتدء انجساحج يالحظج انىسيط يالحظىج إن يعبعلبح يب ة د انجساحج نهسظ انصبةي ةب يجب ي بنجذ

يصيقج ة د انجساحج يتبعسث نذقهيم األثبز انسهتيج نر انذيج انصبحتج نسظ زو ان انسحبئ .