Evaluation of glial tumors: correlation between magnetic resonance imaging and histopathological analysis

Campos, Lillian Gonçalves; Oliveira, Francine Hehn de; Antunes, Ápio Cláudio Martins; Duarte, Juliana Ávila

doi:10.1590/0100-3984.2024.0025

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Original Article • Radiol Bras 57 • 2024 • https://doi.org/10.1590/0100-3984.2024.0025 copy

Evaluation of glial tumors: correlation between magnetic resonance imaging and histopathological analysis

Avaliação de tumores gliais por ressonância magnética e correlação com estudo histopatológico

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Objective:

To determine the correlation of conventional and diffusion-weighted imaging findings on magnetic resonance imaging (MRI) of the brain, based on Visually AcceSAble Rembrandt Images (VASARI) criteria, with the histopathological grading of gliomas: low-grade or high-grade.

Materials and Methods:

Preoperative MRI scans of 178 patients with brain gliomas and pathological confirmation were rated by two neuroradiologists for tumor size, location, and tumor morphology, using a standardized imaging feature set based on the VASARI criteria.

Results:

In the univariate analysis, more than half of the MRI characteristics evaluated showed a significant association with the tumor grade. The characteristics most significantly associated with the tumor grade were hemorrhage; restricted diffusion; pial invasion; enhancement; and a non-contrast-enhancing tumor crossing the midline. In a multivariable regression model, the presence of enhancement and hemorrhage maintained a significant association with high tumor grade. The absence of contrast enhancement and restricted diffusion were associated with the presence of an isocitrate dehydrogenase gene mutation.

Conclusion:

Our data illustrate that VASARI MRI features, especially intratumoral hemorrhage, contrast enhancement, and multicentricity, correlate strongly with glial tumor grade.

Keywords:
Glioma; Neoplasm grading; Magnetic resonance imaging; Brain neoplasms; Isocitrate dehydrogenase

MRI sequence	Parameter	1.5-T scanner	3.0-T scanner
Axial T2-weighted spin-echo FLAIR	Slice thickness	5.0 mm	4.0 mm
	Pixel/voxel size	0.9 X 0.9 mm	1.1 X 1.1 mm
	Echo time	140 ms	135 ms
	Repetition time	11,000 ms	8,000 ms
	Inversion time	2,200 ms	2,400 ms
	Acquisition matrix	256 X 256	512 X 512
Axial T1-weighted spin-echo	Slice thickness	5.0 mm	4.5 mm
	Pixel/voxel size	0.8 X 0.8 mm	0.9 X 0.9 mm
	Echo time	15 ms	13 ms
	Repetition time	616 ms	660 ms
	Acquisition matrix	256 X 256	512 X 512
Axial T2-weighted spin-echo	Slice thickness	5.0 mm	4.0 mm
	Pixel/voxel size	0.5 X 0.5 mm	0.6 X 0.6 mm
	Echo time	100 ms	92 ms
	Repetition time	5,655ms	3,000 ms
	Acquisition matrix	256 X 256	576 X 576
Axial contrast-enhanced three-dimensional T1-weighted gradient-echo	Slice thickness	2.0 mm	1.0 mm
	Pixel/voxel size	0.7 X 0.7 mm	1.0 X 1.0 mm
	Echo time	3.79 ms	3.5 ms
	Repetition time	25 ms	7.9 ms
	Acquisition matrix	352 X 352	512 X 512
Axial echo-planar DWI with ADC mapping	Slice thickness	3.5 mm	3.5 mm
	Pixel/voxel size	0.7 X 0.7 mm	1.79 X 1.79 mm
	Echo time	77.6 ms	117 ms
	Repetition time	6,629 ms	5,852 ms
	Acquisition matrix	336 X 336	432 X 432

Features and scoring	Definition

Major axis size 1. 0.5-5.0 cm; 2. > 5.0 cm	The diameter of the tumor on its longest axis
Tumor location 1. Lobar^*; 2. Other locations^†	Location of the geographic epicenter of the lesion ^* Frontal, temporal, parietal, occipital, insular;^† basal ganglia, brainstem, cerebellum, thalamus
Side of tumor epicenter 1. Right or left; 2. Bilateral/central	Laterality of the lesion epicenter
Eloquent brain area^* involvement 1. Yes; 2. No	Does the geographic epicenter or the enhancing component involve an eloquent area of the brain? ^* Speech motor, speech receptive, motor, vision
Enhancement quality 1. None; 2. Minimal^; 3. Marked^	Qualitative degree of contrast enhancement ^* Grouped so that the presence of enhancement is in a single category
Proportion CET 1. 0%^; 2. < 5%^; 3. 6-33%^*; 4. 34-67%^†; 5. 68-95%^†; 6. > 95%^†	Assuming that the entire abnormality may be comprised of an enhancing component, a non-enhancing compo-nent, a necrotic component, and an edema component, what proportion of the tumor is enhancing? ^* 0-33% (grouped categories);^† > 34% (grouped categories)
Proportion nCET 1. 0%^; 2. < 5%^; 3. 6-33%^; 4. 34-67%^; 5. 68-95%^†; 6. > 95%^†	An nCET is defined as regions of T2WI hyperintensity (less than the intensity of the cerebrospinal fluid, with cor-responding T1WI hypointensity. In view of that, what proportion of the tumor is non-enhancing? ^* 0-33% (grouped categories);^† > 34% (grouped categories)
Proportion necrosis 1. 0%^; 2. < 5%^; 3. 6-33%^†; 4. 34-67%^†; 5. 68- 95%^†; 6. > 95%^†	Defined as a region within the tumor that does not enhance or shows markedly diminished enhancement, with hyperintensity on T2WI, hypointensity on T1WI, and an irregular border ^* < 5% (grouped categories); ^†> 5% (grouped categories)
Cysts 1. Yes; 2. No	Well-defined, rounded, often eccentric regions of very high and low signal intensity on T2WI and T1WI, respec-tively, essentially matching that of the cerebrospinal fluid, with very thin, regular, smooth, non-enhancing or regularly enhancing walls, possibly with thin, regular, internal septations
Multifocal or multicentric 1. No; 2. Multifocal^; 3. Multicentric^; 4. Gliomatosis^*	Multifocal is defined as having at least one region of tumor, either enhancing or non-enhancing, which is not contiguous with the dominant lesion. Multicentric is defined as widely separated lesions in different lobes or dif-ferent hemispheres. Gliomatosis refers to the generalized neoplastic transformation of the white matter of most of a hemisphere ^* Grouped into one category
Tl/FLAIR ratio 1. Expansive; 2.Mixed^; 3. Infiltrative^	Expansive = size of the abnormality on an unenhanced T1WI approximates that seen on a FLAIR sequence. Mixed = size of the abnormality on an unenhanced T1WI moderately less than that seen on a FLAIR sequence. Infiltrative = size of the abnormality on an unenhanced T1WI much smaller than that seen on a FLAIR sequence ^* Grouped into one category
Thickness of enhancing margin 1. Not applicable; 2. None; 3. Thin; 4. Thick	The scoring is not applicable if there is no contrast enhancement. If most of the enhancing rim is thin, regular, and homogenous, the grade is thin. If most of the rim demonstrates nodular or thick enhancement, the grade is thick. If there is only solid enhancement and no rim, the grade is none
Definition of enhancing margin 1. Not applicable; 2. Well-defined; 3. Poorly defined	The score is not applicable if there is no contrast enhancement. Assess if most of the outside margin of the en-hancement is well defined or poorly defined
Definition of the non-enhancing margin 1. Smooth; 2. Irregular; 3. Not applicable	If most of the outside non-enhancing margin of the tumor is well defined and smooth (geographic), versus poorly defined and irregular
Proportion of edema 1. 0%^; 2. < 5%^; 3. 6-33%^t; ; 4. 34-67%^†; 5. 68-95%^†; 6. > 95%^†	What proportion of the abnormality is vasogenic edema? Edema should be greater in signal than nCET ^* < 5% (grouped categories);^† > 5% (grouped categories)
Edema crossing the midline 1. Yes; 2. No	Edema spans white matter commissures extending into the contralateral hemisphere
Hemorrhage 1. No; 2. Yes	Intrinsic hemorrhage in the tumor matrix. Any intrinsic foci of low signal intensity on T2WI and SWI or high signal intensity on T1WI
Diffusion 1. Facilitated^; 2. Restricted; 3. Neither/equivocal^	Predominantly facilitated or restricted diffusion in the enhancing or non-enhancing portion of tumor. (Based on the ADC map). The proportion of tissue is not relevant ^* Grouped into one category
Pial invasion 1. Yes; 2. No	Enhancement of the overlying pia in continuity with CET or nCET
Ependymal invasion 1. Yes; 2. No	Invasion of any adjacent ependymal surface in continuity with CET or nCET matrix
Cortical involvement 1. Yes; 2. No	CET or nCET extending to the cortical mantle, or cortex is no longer distinguishable relative to the subjacent tumor
Deep white matter invasion 1. Yes; 2. No	CET or nCET extending into the internal capsule or brainstem
nCET crossing the midline 1. Yes; 2. No	nCET crosses into the contralateral hemisphere through white matter commissures
CET crossing the midline 1. Yes; 2. No	Enhancing tissue crosses into the contralateral hemisphere through white matter commissures
Satellites 1. Yes; 2. No	A satellite lesion is an area of enhancement within the region of signal abnormality surrounding the dominant lesion but not contiguous in any part with the major tumor mass

Variable	(N = 178)
Histopathological grade, n (%)
High	140 (78.7)
Low	38 (2.3)
Sex, n (%)
Female (all)	76 (42.7)
Female with a high-grade tumor	53 (69.7)
Female with a low-grade tumor	23 (30.3)
Age (years), mean ± standard deviation
All patients	53.7 ± 14.6
Patients with a high-grade tumor	55.8 ± 13.7
Patients with a low-grade tumor	46.1 ± 15.7
Histological type, n (%)
Glioblastoma	111 (62.4)
WHO grade 2 astrocytoma	19 (10.7)
WHO grade 3 astrocytoma	16 (9.0)
Other	32 (17.9)
Immunohistochemistry, n (%)
IDH mutation	47 (26.0)
Ki-67	76 (42.7)

Feature	n (%)
Tumor location
Lobar	119 (66.9)
Other (deep)	59 (33.1)
Necrosis
Yes	161 (90.4)
No	17 (9.6)
Deep white matter invasion
Yes	76 (57.3)
No	102 (42.7)
Enhancement
Yes	153 (86.0)
No	23 (13.9)
Laterality
Right/left	157 (88.2)
Central/bilateral	21 (11.8)
CET crossing the midline
Yes	36 (20.2)
No	140 (78.7)
Multicentric/multifocal
Yes	41 (23.0)
No	137 (77.0)
Cysts
Yes	18 (10.1)
No	160 (89.9)
nCET crossing the midline
Yes	84 (47.2)
No	94 (52.8)
Tl/FLAIR
Expansive	53 (30.0)
Infiltrative	125 (70.0)
Edema crossing the midline
Yes	74 (41.6)
No	104 (58.4)
Satellite lesions
Yes	36 (20.2)
No	140 (78.7)
Edema proportion
<5%	149 (83.7)
>5%	29 (16.3)
Hemorrhage
Yes	117 (65.7)
No	58 (41.6)
Cortical involvement
Yes	136 (76.4)
No	42 (23.6)
Restricted diffusion
Yes	47 (26.4)
No	126 (70.8)
Pial invasion
Yes	61 (34.3)
No	115 (64.6)
Eloquent brain area
Yes	59 (33.1)
No	119 (66.9)
Diameter
0.5-5.0 cm	60 (33.7)
> 5.0 cm	118 (66.3)
Ependymal invasion
Yes	123 (69.1)
No	55 (30.9)
Enhancement proportion
0-33%	131 (73.6)
34-100%	45 (25.3)
Perfusion^* * Data available for only 84 (47.2%) of the 178 patients.
Increased	63 (75.0)
Decreased	21 (25.0)

Variable	OR	95% Cl	P-value
Deep tumor	1.5	0.68-3.4	0.3
Central/bilateral	2.8	0.63-12.7	0.16
Eloquent area	0.9	0.4-2.0	0.8
No cysts	3.5	1.3-9.5	< 0.01
Infiltrative	0.5	0.2-1.1	0.08
Edema crossing the midline	2.4	1.07-5.2	< 0.05
Hemorrhage	7.1	3.2-15.7	< 0.01
Restricted diffusion	2.7	1.0-7.5	< 0.01
Pial invasion	5.9	2.0-17.8	< 0.01
Ependymal invasion	1.6	0.78-3.4	0.2
Cortical involvement	0.5	0.21-1.4	0.2
Deep white matter invasion	1.3	0.6-2.8	0.4
nCET crossing the midline	3.2	1.4-6.9	< 0.01
CET crossing the midline	3.7	1.06-12.7	< 0.05
Satellite lesions	3.6	1.06-12.7	< 0.05
Enhancement	10.6	4.0-27.8	< 0.01
Multifocal/multicentric	3.0	1.0-9.2	< 0.05
Necrosis	1.2	0.3-3.7	0.8
Necrosis proportion > 5%	7.2	3.2-16.0	< 0.01
Edema proportion > 5%	9.2	1.2-70.3	< 0.01
Enhancement proportion > 34%	2.9	1.0-7.4	< 0.05
Non-enhancement proportion < 67%	3.9	1.4-10.5	< 0.01
Diameter > 5.0 cm	0.9	0.4-1.9	0.75

Variable	OR	95% Cl	P-value
No cysts	0.3	0.1-1.1	0.07
Edema crossing the midline	1.07	0.3-3.6	0.9
Hemorrhage	3.1	1.2-8.6	< 0.05
Pial invasion	2.6	0.7-9.1	0.14
nCET crossing the midline	1.3	0.3-5.4	0.7
CET crossing the midline	1.3	0.3-7.0	0.7
Satellite lesions	1.5	0.4-6.7	0.5
Enhancement	3.1	1.0-10.4	< 0.05
Multifocal/multicentric	2.3	0.5-9.7	0.2
Edema proportion > 5%	3.9	0.45-32.0	0.2
Non-enhancement proportion < 67%	2.3	0.7-7.3	0.18
Necrosis proportion > 5%	2.0	0.6-8.5	0.2
Restricted diffusion	1.4	0.4-4.8	0.6
Enhancement proportion > 34%	0.4	0.1-2.3	0.3

Variable	OR	95% Cl	P-value
Hemorrhage	3.6	1.3-9.1	< 0.01
Pial invasion	2.9	0.8-9.5	0.08
Enhancement	4.3	1.4-12.8	< 0.01
Multifocal/multicentric	3.5	1.0-11.9	< 0.05

Variable	OR	P-value
No hemorrhage	1.2	0.75
Decreased perfusion^* * Data available for only 21 (11.8%) of the 178 patients.	4.0	0.6
No enhancement	17.0	< 0.01
Lobar location	1.7	0.5
No multifocality	4.4	0.15
No pial invasion	2.0	0.4
No restricted diffusion	3.9	<0.05

Variable	P-value
CET crossing the midline	0.5
Edema crossing the midline	0.5
Hemorrhage	0.19
Pial invasion	< 0.05
nCET crossing the midline	0.8
Satellite lesions	0.7
Enhancement	0.4
MuIticentric/muItifocal	< 0.05

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[1] Correspondence
: Dra. Lillian Gonçalves Campos. Hospital de Clínicas de Porto Alegre, Departamento de Radiologia. Rua Ramiro Barcelos, 2350, Santa Cecília. Porto Alegre, RS, Brazil, 90035-903. Email: lilliancamposradiologia@gmail.com