EL-MINIA MED. BULL. VOL. 21, NO. 2, JUNE, 2010
Mohsen et al
ADVANCED MRI IN THE GRADING OF GLIOMA
By
Laila Adel MS Mohsen*, Osama AW Khalil*,
Hosny SA Ghany* and Jonathan H Gillard**
Departments of *Radiology, El-Minia University, El-Minia, Egypt,
And **Radiology, Cambridge University, Cambridge, UK
ABSTRACT:
Introduction: The highly variable appearance of gliomas on conventional MRI has
always been troublesome for radiologists and clinicians. The typical diagnosis of
higher grade gliomas is still based upon the contrast enhancement of the thick ring of
tumor tissue surrounding a central degenerated zone. This enhancement is well known
to reflect only an altered blood brain barrier which is not related histologically to
tumor grade.
Aim of study: to evaluate the role of advanced MRI techniques in the grading of
cerebral glioma.
Patients and Methods: 39 patients were included in this study, where 30 patients had
GBM and 9 patients had grade II oligo-dendrogliomas. All patients also had a
standard pre-operative anatomical MRI sequence and additional DTI, MRS and DSC
imaging sequences, using a standard 8-channel head coil. Those patients were imaged
on a 3T MRI scanner (MAGNETOM TrioTim, Siemens Medical Systems, Erlangen,
Germany). Images were analyzed using dedicated post-processing software packages.
Results: The mean±SD minimum ADC value for the HGG tumors was 0.46±0.11
x10-3 mm2/s, while for the LGG, the mean±SD minimum ADC was 0.4±0.27 x10-3
mm2/s. The difference in minimum ADC value was not significant between both
patient groups (p = 0.41). The mean±SD maximum normalized rCBV value for HGG
tumors was 6.5±2.6, while for the LGG patients, it was 3.6±0.6. The difference
between them was significant (p = 0.007). The MRS ratios were not significantly
different between both grades.
Conclusion: Advanced MRI techniques offered additional evidence for the purpose
of pre-operative grading of gliomas. However, Perfusion MRI and MRS were more
successful for this purpose than DTI.
especially now with the increasing
identification of several and newer
subtypes of glioma, e.g. papillary glioneuronal tumor (PGNT).1 These have
been proven by many studies to be
non-specific signs. This necessitates
the evaluation of physiological imaging modalities where high and low
grade tumors can be differentiated.
INTRODUCTION:
Conventional imaging has for
long time depended upon contrast
enhancement as the primary indicator
of high grade tumors or transformation
of low grade tumors into high grade
ones. It is principally caused by poorly
formed, leaky blood vessels with a
damaged blood brain barrier. And
although enhancement, hemorrhage,
necrosis, peritumoral edema and mass
effect upon neighboring structures are
classic features of GBM, yet LGGs can
also present with similar features,
The aim of this study is to
evaluate the role of advanced MRI
techniques in the grading of cerebral
glioma.
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confirmed by biopsy. The patients
were scanned at different time periods.
The patients were scanned at the time
period of July 2010 to July 2011. The
LGG group of patients was taken from
archive and had standard sequences.
Their available images were as
follows:
PATIENTS AND METHODS:
Patients:
This study was conducted in the
MRIS (MRI & Spectroscopy) unit and
WBIC (Wolfson Brain Imaging
Center), Addenbrooke’s hospital,
Cambridge, UK. It included 39
patients, all of whom had GBM,
Table 1: Distribution of sequences for LGG patients:
LGG patients
1
2
3
4
5
6
7
8
9
DWI
*
*
*
*
*
PWI
*
*
*
*
*
MRS
*
*
*
* (SVS)
* (CSI)
* (CSI)
* (CSI)
4. Diffusion Tensor Imaging with
the following parameters: axial slices,
single-shot SE-EPI, TR/TE: 8k/98 ms,
NEX: 1, slice thickness/inter-slice gap:
2/2 mm, resolution 256x256, 12
directions, other than the b0, five bvalues were used (350, 650, 1000,
1300 and 1600 s/mm2), FOV:
153.6x153.6 cm.
5. Dynamic
Susceptibility
Contrast (DSC) perfusion imaging with
the following parameters: axial GRE
slices, TR/TE: 1500/30 ms, NEX: 1,
Flip angle: 90°, FOV: 192x192 mm,
resolution:
96x96,
with
90
measurements. After the 10th measurement, contrast was bolus injected and
followed by saline flush.
6. Similarly, the contrast given is
Magnevist (Schering, Germany) and it
is given as a standard dose for all
patients. The dose given is 9 ml that is
followed by 20 ml saline flush.
MR Imaging
All patients also had a standard preoperative anatomical MRI sequence
and additional DTI, MRS and DSC
imaging sequences, using a standard 8channel head coil. Those patients were
imaged on a 3T MRI scanner
(MAGNETOM TrioTim, Siemens
Medical Systems, Erlangen, Germany).
The MR study included:
1. Axial pre-contrast T1-weighted
(TR/TE: 500/8 msec, NEX: 1, slice
thickness/inter-slice gap: 4/5 mm,
resolution: 320x256, FOV: 19x24 cm).
2. Axial T2-PD (TR/TE1/TE2:
4600/ 12/104 ms, NEX: 1, slice
thickness /inter-slice gap: 4/5 mm,
resolution: 320x240, FOV: 19x24 cm).
3. Axial FLAIR (TR/TE/TI: 7840/
95/2500 ms, NEX: 1, slice thickness/
inter-slice gap: 4/5 mm, resolution:
320x256, FOV: 20x25 cm).
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7. Post-contrast
MPRAGE
sequence (TR/TE: 19/5, NEX: 1, FOV:
25.6x25.6x25.6
cm,
matrix:
180x220x256
interpolated
to
256x256x256 sections for reconstruction; 1mm section thickness).
8. Axial T2 weighted turbo spin
echo (T2-TSE) sequence was the
sequence used to plan the MRS. It had
the following parameters: (TR/TE:
4840/114 msec, NEX: 1, ETL: 19,
slice thickness/inter-slice gap: 5/5 mm,
resolution:320x168,FOV:16.5x22 cm).
9. Magnetic Resonance Spectroscopy (MRS) with the following
parameters: Two MRS scans were performed, the first with water supperssion and the second without water
suppression. Multi-Voxel Spectroscopy (MVS) was used with PRESS
acquisition. Single axial slice was
chosen to include as much of the solid
tumor and peri-tumoral region as
possible. TR/TE: 2000/35 ms, NEX: 3
for water suppressed sequence and 1
for the unsuppressed sequence, FOV:
16x16 cm and slice thickness is 2 cm.
The individual voxel size was
10x10x20 mm. The water suppressed
metabolite sequence was done first to
be followed by the non-water suppressed sequence and both of them
followed contrast injection and
volumetric MPRAGE imaging. It has
been confirmed by many researchers
that the effect of contrast medium upon
the quality of the spectra is negligible.
Mohsen et al
MD 
FA=
1  2  3
3
(2)
For the ADC & FA map, a
large Region of Interest (ROI) was
used to encase as much as possible of
the solid tumor tissue. For slices which
show a degenerated center or susceptibility artifacts, we used multiple
smaller ROIs to encase only the solid
tumor tissue away from those two
components. The measurements from
all ROIs were saved and then the
smallest ADC value was used.3
Analysis of the perfusion
images was the next step, where the
DSC perfusion image set was
processed by Nordic Ice software
(Nordic Neuro Lab, Norway) to extract
the rCBV map. The perfusion images
are analyzed by the program and the
signal intensity – time (T2* susceptibility) curve is calculated. Automatic
correction of contrast leakage was
done and a gamma variate function
applied to the curve. The rCBV map
was then automatically produced. The
evaluation of rCBV maps was done
after identifying the regions of large
feeding vessels so that they are avoided
from ROI placement (over-estimation
of rCBV).4 The maximum rCBV value
was recorded and then normalized to
the contralateral side.
Image Processing
The
DTI
images
were
processed using FSL (FMRIB, Oxford,
UK). Using brain extraction tool
(BET), the skull was stripped off the
main diffusion file. Then various DTI
parameters were extracted. Mean
Diffusivity (MD) and Fractional
Anisotropy (FA) maps are calculated
automatically according to the
following formulae:
The analysis of the MRS
spectra was the last step. For this we
used the commercial software of the
MR machine. The software gives an
estimate of the concentration of the
metabolite (being directly proportional
to the area under the peak) as well as
the ratio of the metabolite to Cr.
Spectral voxels that cover the main
tumor bulk were used for the grading
step. The metabolites used were
NAA:Cr, Cho:Cr, Ins:Cr and Glx:Cr.
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The lipid & lactate peak was not used
because of the expected overlapping of
both metabolites.
Mohsen et al
The mean age of all patients
included in our study was 55.7 years
with a range of 20–74 years. The age
mean and SD for the HGG group was
58.7 ± 9.6 years, while for the LGG
group it was 34 ± 14.6 years. The LGG
was significantly more common in
younger patients than HGG. (p <
0.0001).
Statistical Analysis:
Statistical analysis was done using
SPSS PC version 16 for Windows
(SPSS, Cary, NC). All numbers were
normally distributed. Independent
sample t-test was used to compare the
ADC, FA, rCBV and different
metabolite ratios between HGG and
LGG. A level of significance is
considered if the p value is less than
0.05.
The study included 44 (74.6%)
male patients and 15 (25.4%) female
patients. Within the HGG group, there
were 37 male patients and 13 female
patients, while within the LGG group;
there were 7 male patients and 2
female patients only. Again, there was
no significant variation in the sex
distribution among both groups. (p =
0.89).
RESULTS:
This study included 39 patients
in total, 30 of whom had GBM,
confirmed by biopsy and 9 patients had
LGG.
Table 2: Demographic characteristics of patients:
Characteristic
Age (Mean ± SD)
Sex:
Male
Female
Total number of patients
HGG
58.7 ± 9.6
LGG
34 ± 14.6
27
3
30
7
2
9
about 0.69±0.18 x10-3 mm2/s. The
difference in minimum ADC value was
not significant between both patient
groups (p = 0.41), even after
normalization (p = 0.67). The mean FA
value was 0.15 for both groups (p =
0.94). All measures were significantly
different from the contralateral side. (p
< 0.005)
1. ADC and FA:
The mean±SD minimum ADC
value for the HGG tumors was
0.46±0.11 x10-3 mm2/s, while for the
LGG, the mean±SD minimum ADC
was 0.4±0.27 x10-3 mm2/s. Normalized
ADC values for the HGG patients
measured about 0.7±0.17 x10-3 mm2/s,
and for the LGG patients, it measured
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Figure 1: Boxplot of the minimum ADC values for each of the 2 patient groups and
revealing marked overlap between both categories.
Table 3: Description of the main DTI parameters used for grading glioma and the
difference between both groups:
Measures
evaluated
Min ADC (x10-3)
rADC (x10-3)
Mean FA
HGG (30)
LGG (5)
p-value
0.46±0.11
0.7±0.17
0.15±0.06
0.4±0.27
0.69±0.18
0.15±0.07
0.74
0.91
0.94
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B
A
C
Mohsen et al
D
E
Figure 2: A) T2 weighted image revealing a left temporo-parietal GBM, with a
heterogeneous appearance of solid components and degenerated parts, mainly in the
center as well as susceptibility artifact from old hemorrhagic parts. B) Contrast
enhanced T1 weighted image revealing the thick enhancing rind of active tumor
tissue. C) ADC map revealing the same heterogeneous appearance of restricted and
enhanced diffusion as well as the susceptibility artifact caused by hemosiderin. D)
Color-coded FA map revealing the interruption of the white matter fibers in the region
of the tumor as well as the left external capsule. The surrounding fibers (posterior
limb of internal capsule) show decreased anisotropy (color hue) suggesting they are
infiltrated by tumor cells. E) FA map showing the same appearance as the color-coded
map but with less appreciation of the infiltrated fibers surrounding the tumor.
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2. rCBV:
For this assessment, 5 patients
with low grade glioma were included, all
of whom were WHO grade 2 oligodendrogliomas. The mean±SD maximum
normalized rCBV value for HGG tumors
was 6.5±2.6, while for the LGG patients,
it was 4.42±1.5. The difference between
them was significant (p = 0.007).
A
B
C
D
Figure 3: A & B represent contrast enhanced T1-weighted (A) and rCBV map (B) of
a left frontal WHO grade 2 glioma, while C & D represent contrast enhanced T1weighted (A) and rCBV map (B) of a right frontal GBM. In B, we can see a small
focus of increased vascularity in the periphery of the tumor; on revision of the raw
DSC images, it was realised that this focus was due to a feeding vessel to the tumor.
In D, we can see the entire tumor periphery showing increased vascularity but the
cortical regions were caused by feeding cortical vessels; on the contrary, the inner
regions were caused by active tumor tissue and increased cerebral blood volume.
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2. MRS:
The basic metabolites that were
assessed are total NAA, total Cho, myoInositol and Glutamates. Each of these
metabolites was referenced to the total
Cr for the same voxel and for the average
total Cr of the contra-lateral hemisphere.
Total Cho was also referenced to the
total NAA of the same voxel.
Mohsen et al
For this analysis, 5 patients with
LGG were included for the analysis but
only 1 patient of this group had SVS,
accordingly the ratios normalized to the
contra-lateral side were not included for
this patient. The difference between
HGG and LGG was more remarkable
using the myo-Inositol to Creatine ratios,
however, the difference did not reach
significance.
Table 4: Mean±SD of the ratios used for grading of gliomas:
Ratio
LGG
HGG
1.18±0.68
1.03±0.65
NAA/Cr
2.1±1.07
5.02±3.9
Cho/Cr
2.15±1.5
4.13±3.58
Cho/NAA
2.02±1.44
0.38±0.32
Ins/Cr
1.35±0.89
1.91±2.61
Glx/Cr
p value
0.72
0.17
0.53
0.098
0.7
A
B
Figure 4: MR Spectrum from a GBM patient
without lipid/lactate peak revealing the
prominently increased Cho peak (3.2 ppm)
with a Cho/Cr ratio of 1.3. No myo-Inositol
peak (3.56 ppm) could be appreciated. The
NAA peak (2.02 ppm) is reduced with a
NAA/Cr ratio of 0.8.
Figure 5: Spectrum from WHO grade
2 glioma revealing the elevated Cho
peak (3.2 ppm) with a Cho/Cr ratio of
0.52, reduced NAA peak (2.02 ppm)
with a NAA/Cr ratio of 0.51, increased
lac/lipid peak (0.7-1.6 ppm) as well as
an increased Ins peak (3.56 ppm) with
an Ins/Cr ratio of 2.99.
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However; we were unable to
reproduce these results. We found
remarkable overlap of values between
both categories. In this we agreed with
Rollin et al, Lam et al. and Kono et
al.5,11,12
DISCUSSION:
Conventional imaging has been
for long time and is still dependent
upon contrast enhancement as the
primary indicator of high grade tumors
or transfor-mation of low grade tumors
into high grade ones. It is principally
caused by poorly formed, leaky blood
vessels with a damaged blood brain
barrier. Enhancement, hemorrhage,
necrosis, peritumoral edema and mass
effect upon neighboring structures are
all non-specific signs. Excessive work
has been and is still ongoing to
establish a reliable method for preoperative glioma grading based upon
the advanced MR modalities.
Perfusion MR:
Regional
cerebral
blood
volume (rCBV) also strongly correlates
to tumor grade.13-16 There are 3 main
vascular histological phenomena that
accompany
glioma
development.
These are neo-angiogenesis, vascular
“intussusception” (which means the
infiltration of vascular intima and
interstitial tissue by tumor cells) and
vascular cooption which is the
recruitment of local blood vessels by
the tumor. These factors lead to
increased blood volume in the tumor
bed and edges.17 This direct relation to
tumor grade is stronger after the
exclusion of oligodendroglioma and
pilocytic astrocytoma. Although both
types are low grades, yet they have
exceptionally high rCBV values which
confounded the results of some studies.
In our study, we had only 5 patients
with low grade gliomas, all of whom
were oligodendrogliomas. The mean
normalized rCBV value for this group
of patients was 4.42±1.5. This agrees
with Cha et al who compared low
grade astrocytoma to low grade oligodendroglioma and revealed that the
mean rCBV for oligodendroglioma
could be more than twice that for low
grade astrocytoma. In spite of this high
rCBV, we had a significant difference
between glioblastoma and low grade
oligo-dendrogliomas, where in glioblastomas, the mean normalized rCBV
was 6.5±2.6.18
ADC Mapping:
Higher mitotic activity and
cellularity are associated with higher
grades of glioma. With higher cellularity, the extracellular water diffusion
becomes increasingly restricted. This
has been proven by many authors using
DWI and ADC mapping, where the
lower ADC values correlated greatly
with tumor cellularity.5-8 Stadnik et al.
reported a mean ADC value of 1.14 x
10-3 mm2s-1, Sugahara reported 1.2±0.4
x 10-3 mm2s-1, whereas Calli et al and
Kono et al reported a mean ADC for
the solid tumor components of
0.92±0.28 x 10-3 mm2s-1.3,5,6,9 The
small difference between those results
is probably due to the exclusion of
necrotic and cystic components from
the measurement in the second group,
as well as the choice of the minimum,
and not the mean ADC of the ROIs.
Our results were closer to the later
authors, where the mean minimum
ADC for HGG was 0.46±0.11 x 10-3
mm2s-1 and 0.43±0.24 x 10-3 mm2s-1
for LGG. Many authors reported
significantly higher ADC values for
LGG than HGG and even used a cutoff value of reasonable sensitivity and
specificity for this discrimination.10
MR Spectroscopy:
We had the greatest separation
between both grades using the myoInositol ratios to creatine, yet it didn’t
achieve significant differentiation
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between both grades. This could have
been due to the low number of LGG
patients. Castillo et al suggested that
myo-Inositol was increased in LGG
that in control healthy subjects and is
much lower than normal in grades III
and IV.19 He reported the values of
0.82±0.25 for LGG versus 0.15±0.12
for GBM. Our results were different
from his where we found the mean
Ins/Cr ratio for LGG to be 2.02±1.44,
while for HGG, it was 0.38±0.32. The
difference between our results and his
could be due to a number of causes.
First, his group of patients included
some patients who received some kind
of previous therapy and had recurrent
lesions. Second, he suggested that Cr is
a relatively stable metabolite between
healthy and diseased tissue, yet recent
work has proved that Cr does change
significantly between healthy tissue
and tumors.20-22
could vary remarkably.14 Again we
couldn’t reproduce these results which
could also be due to the low number of
LGG patients.
The high Cho levels were
found to correlate strongly with tumor
proliferative activity and MIB index.23
The mean Cho/Cr ratio in our study
was 5.02±3.9 for HGG and 2.1±1.07
for LGG. Some authors have also
failed to reach significant differenttiation between high and low grade
tumors using Cho/Cr.24 We believe this
was mainly because of the low number
of low grade glioma patients,
especially when our group of patients
was composed entirely of oligodendrogliomas.
The heterogeneity of gliomas
and the significant overlap of values
between all grades hindered the utility
of ADC mapping in pre-operative
grading.
Conclusions:
Low grade gliomas have good
prognosis with longer survival, while
glioblastomas, on the other hand, have
the worst prognosis and shortest
survival. Planning a patient’s treatment
necessitates the pre-operative identifycation of the pathology of the tumor
and its extension. In our study, we
were successful at grading tumors
using rCBV analysis. Although we
were not similarly successful with
MRS, we believe that MRS is valuable
in pre-operative grading of gliomas.
But we still need more work to
establish a reliable method for
evaluation of the enormous output that
we get from spectroscopy.
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21. Meyerand ME, Pipas JM,
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Mohsen et al
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‫الملخص العربي‬
‫) هي األورام الخبيثة الناشئة من الخاليا الدبقية وهي خاليا‬Glioma( ‫االورام الدبقية‬
‫ من جميع األورام‬٪03 ‫ الى‬03 ‫ تمثل هذه األورام حوالي‬.‫مساعدة تحيط بخاليا الجهاز العصبي‬
‫ الدرجة‬.‫ وتقسم هذه األورام الى أربعة درجات طبقا لمعدالت نموها‬.‫األولية داخل الجمجمة‬
‫األولى والثانية تتسم بمعدل نمو بطئ أما الدرجات الثالثة والرابعة فمعدل نموها سريع وبالتالي‬
.‫لها مضاعفات أكثر وأسوأ في بعض المرضى وتؤدي في النهاية الى الوفاة‬
‫يعتبر تشخيص األورام الدبقية وتحديد درجتها بدقة من أهم المشاكل التي واجهت‬
‫ وقد اتفق أعضاء الجمعية االميركية لجراحي المخ واألعصاب على أن التحليل‬.‫العلماء‬
‫الباثولوجي للعينة النسيجية المأخوذة من الورم هي المعيار األدق لتشخيص نوع الورم وتحديد‬
‫ ولكن هناك بعض السلبيات لالعتماد فقط على‬.‫ وبالتالي وضع البروتوكول العالجي له‬،‫درجته‬
‫ فالورم الدبقي من‬.‫أخذ عينة نسيجية للتشخيص النهائي وبناء القرار العالجي على أساس نتائجها‬
‫ هذا يؤدي الى أن أخطاء أخذ العينات النسيجية‬.‫الدرجة الرابعة هو ورم غير متجانس للغاية‬
‫ مما يؤدي الى‬،‫واردة الحدوث ويمكن للعينة أن تصيب جزءا أقل درجة من جزء اخر للورم‬
.‫تشخيص درجة أقل للورم وهو ما يترتب عليه اختيار عالج غير مناسب للمريض‬
‫يعتبر التصوير بالرنين المغناطيسي الفحص األساسي للمرضى الذين يشتبه في اصابتهم‬
.‫ وهو فحص مهم للغاية ليس فقط لتشخيص المرض وانما أيضا لتخطيط العملية‬.‫بأورام المخ‬
‫ويعتمد التشخيص بالرنين المغناطيسي في العادة على رؤية الورم في وسط األنسجة الطبيعية‬
209
‫‪Mohsen et al‬‬
‫‪EL-MINIA MED. BULL. VOL. 21, NO. 2, JUNE, 2010‬‬
‫وضغطه لألنسجة المحيطة به‪ .‬أما وجود بؤر نزفية أو نخر وتأثر الورم بالصبغة التي تحقن‬
‫للمريض‪ ،‬فذلك من عالمات ارتفاع درجة خبث الورم‪ .‬ولكن األورام الدبقية ليست دائما بهذه‬
‫البساطة‪.‬‬
‫لقد حاولنا في هذه الدراسة تقييم دور التصوير بالرنين المغناطيسي المتقدم في تحديد‬
‫درجة الورم الدبقي‪ .‬اشتملت هذه الدراسة على ‪ 03‬مريضا‪ ،‬كان درجة الورم الرابعة في ‪03‬‬
‫مريضا والباقي درجة منخفضة منشأهم جميعهم من الخاليا الشجيرية‪ .‬وتم فحص جميع‬
‫المرضى بالرنين المغناطيسي التقليدي‪ ،‬وكذلك بعض أو كل فحوصات الرنين المغناطيسي‬
‫المتطورة‪ .‬وتم التركيز في هذه الدراسة على ثالث فحوصات متطورة‪ ،‬أال وهي تصوير‬
‫االنتشار النووي‪ ،‬تصوير التغذية الدموية لألنسجة والتصوير الطيفي‪ .‬قمنا بتقييم دور هذه‬
‫الفحوصات المتطورة في تحديد درجة الورم‪.‬‬
‫وقد وجدنا أن أفضل الفحوصات تحديدا لدرجة خبث الورم هو تصوير التغذية الدموية‬
‫لألنسجة وذلك على الرغم من أن جميع المرضى ذوي الدرجة المنخفضة كانت أورامهم ناشئة‬
‫عن الخاليا الشجيرية وهي المعروفة بزيادة حجم الدم المتدفق لها‪ .‬فقد وجدنا أن حجم الدم‬
‫المتدفق لألورام ذات الدرجة العالية يصل لضعف الحجم المتدفق للدرجات األقل تقريبا‪.‬‬
‫ثم تلى ذلك تحديد نسبة سكر الميوانوزيتول للكرياتين باستخدام التصوير الطيفي‪ .‬لكننا‬
‫لم نستطع تحديد مستوى يمكن االعتماد عليه للفصل بين درجات األورام‪ .‬وقد يكون ذلك راجعا‬
‫الى انخفاض عدد المرضى ذوي األورام المنخفضة الدرجة أو حقيقة أن جميعهم كانت أورامهم‬
‫لها ذات خلية المنشأ أال وهي الخاليا الشجيرية‪ .‬فقد أيدت بعض األبحاث السابقة نتائجنا عندما‬
‫اقترح أحد الباحثين أن األورام الدبقية العالية الدرجة تتشابه مع تلك المنخفضة الدرجة ذات‬
‫المنشأ من الخاليا الشجيرية في كل النسب الكيميائية المستنتجة باستخدام التصوير الطيفي‪،‬‬
‫باستثناء الالكتيت والدهون والذين يزيدون بارتفاع درجة خبث الورم لكن هذه الصفة يمكن‬
‫التعرف عليها بسهولة بالتصوير بالرنين المغناطيسي التقليدي‪.‬‬
‫لم نتمكن من العثور على أي تباين قوي بين الدرجتين باستخدام خصائص االنتشار‬
‫النووي أو النسب الكيميائية األخرى‪ ،‬وتتفق هذه النتائج مع نتائج معظم األبحاث األخرى في هذا‬
‫الصدد‪.‬‬
‫كان لهذه الدراسة بعض العيوب‪ ،‬أهمها هو عدم وجود عينة نسيجية من المناطق‬
‫المحددة لتشخيص درجة خبث الورم‪ .‬فقد كان من الممكن أن يساهم تحليل النسيج الخلوي من‬
‫المناطق المحددة بالتصوير الوظيفي في تأكيد نتائج البحث أو اضافة أسباب جديدة لها‪ .‬كما أنه‬
‫لم يتم فحص بعض المؤشرات الحيوية للورم والتي لها تأثير واضح في استجابة المرضى‬
‫للعالج‪.‬‬
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