Lack of the cerebral peduncle involvement in a series of adult supratentorial AVM: a diffusion tensor imaging study.

Abstract

Congenital as arteriovenous malformation(AVM) is, most patients with AVM would be asymptomatic until adults. During the past 2 years, 23 cases of adult supratentorial AVM patients had DTI after admission. The region of interest was placed in the cerebral peduncle. Their FA value and fiber number was compared with those of cavernous malformation (CM) and tumor (glioma and meningioma). In the AVM group, there was no significant difference in FA of the cerebral peduncle (ipsilateral 0.758±0.055 versus contralateral 0.755±0.049; P>0.05) and fiber number (319.6±82.9 versus 304.7±89.1; P>0.05). In the CM group, FA of the cerebral peduncle on ipsilateral side (0.711±0.092) was significantly lower than that of contralateral side (0.768±0.043) (P<0.01). Similar result was in fiber number of the CM group (251±82.1 versus 307.3±77.0; P<0.05). In tumor group, FA of ipsilateral side (0.713±0.084) was lower than that of contralateral (0.751±0.052) without significant difference. There was no significant difference in fiber number between ipsilateral and contralateral sides in the tumor group (308.9±112.4 versus 287.9±62.4). Unlike non-AVM lesions (CM and tumor), FA value and fiber number of the ipsilateral cerebral peduncle is less influenced in the AVM group. The lack of the cerebral peduncle involvement indicates that there is plasticity of white matter in AVM.

Full text

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Neuroscience Letters 486 (2010) 132–135
Contents lists available at ScienceDirect
Neuroscience Letters
journal homepage: www.elsevier.com/locate/neulet
Lack of the cerebral peduncle involvement in a series of adult supratentorial
AVM: A diffusion tensor imaging study
Bing Fua, Jizong Zhaoa,∗, Bo Wangb, Mingqi Yanga, Long Xua, Yan Zhuob
aDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100050, China
bState Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of Sciences, No. 15 Datun Road, Beijing 100101, China
a r t i c l e i n f o
Article history:
Received 24 February 2010
Received in revised form 17 August 2010
Accepted 1 September 2010
Keywords:
Arteriovenous malformation
Cavernous malformation
Cerebral peduncle
Diffusion tensor imaging
a b s t r a c t
Congenital as arteriovenous malformation(AVM) is, most patients with AVM would be asymptomatic
until adults. During the past 2 years, 23 cases of adult supratentorial AVM patients had DTI after admis-
sion. The region of interest was placed in the cerebral peduncle. Their FA value and fiber number was
compared with those of cavernous malformation (CM) and tumor (glioma and meningioma). In the AVM
group, there was no significant difference in FA of the cerebral peduncle (ipsilateral 0.758±0.055 ver-
sus contralateral 0.755±0.049; P>0.05) and fiber number (319.6±82.9 versus 304.7±89.1; P>0.05).
In the CM group, FA of the cerebral peduncle on ipsilateral side (0.711±0.092) was significantly lower
than that of contralateral side (0.768±0.043) (P<0.01). Similar result was in fiber number of the CM
group (251±82.1 versus 307.3±77.0; P<0.05). In tumor group, FA of ipsilateral side (0.713±0.084) was
lower than that of contralateral (0.751±0.052) without significant difference. There was no significant
difference in fiber number between ipsilateral and contralateral sides in the tumor group (308.9±112.4
versus 287.9±62.4). Unlike non-AVM lesions (CM and tumor), FA value and fiber number of the ipsilat-
eral cerebral peduncle is less influenced in the AVM group. The lack of the cerebral peduncle involvement
indicates that there is plasticity of white matter in AVM.
© 2010 Elsevier Ireland Ltd. All rights reserved.
Cerebral arteriovenous malformation (AVM) is usually thought to
be congenital. There were few reports that AVM is de novo [9] or
regresses spontaneously [3]. Hemorrhage, headache, and seizure
arethethreecommonpresentationsincerebralAVM[36].Butmost
patients with AVM would be asymptomatic until adults.
Fractional anisotropy (FA) has been used to characterize water
diffusion anisotropy of brain in diffusion tensor imaging (DTI).
FA depends on organization and myelination of nerve tract [7,8].
Thus, DTI measurements of the cerebral peduncle may be used to
characterize microstructure abnormalities in AVM and non-AVM
lesions. In the present study, we aimed at investigating the cere-
bral peduncle involvement in AVM and non-AVM lesions using
DTI.
Duringthepast2years,therewere51casesofadultwithsupra-
tentoriallesions,includingAVM,cavernousmalformation(CM)and
tumor (glioma and meningioma), who had DTI after admission.
The mean age of the AVM group (n=23) was 33.6 years (range:
21–51 years). Cases of CM (n=14; mean age 37.4 years; range:
20–57 years) and tumors (n=14, 10 cases of glioma and 4 cases
of meningioma; mean age 46.1 years; range: 24–63 years) were
used as control. The ratio of male to female was 15:8, 9:5, and 10:4,
∗Corresponding author. Tel.: +86 010 65113440; fax: +86 010 65113440.
E-mail address: zhaojz@public.bta.net.cn (J. Zhao).
respectively. All lesions were solitary without involvements of the
corpus callosum and the midbrain. Except two patients (one in the
AVM group and one in CM) who could not accept surgical risks,
49 patients underwent operation with informed consent, whose
diagnoses were confirmed by histology.
On a Siemens 3.0 Tesla MRI Scanner, the diffusion-weighted
data were acquired using a single-shot spin-echo diffusion sen-
sitized echo-planar imaging (EPI) sequence with 12 encoding
directions, a diffusion sensitization of b=1000s/mm2, TR of 3s,
and TE of 93ms. EPI image distortion artifacts were reduced using
GRRAPA with acceleration factor or k-space undersampling of
R=2. The slice thickness was 4mm with 22 axial slices covering
the whole brain (foramen magnum to vertex), a field of view of
220mm×220mm,andanimagematrixof128×128thatmatched
sequences described above. The number of image averages was 4.
The total DTI acquisition time was approximately 2.8min.
All of the image processing was performed using the
software MedINRIA (http://www-sop.inria.fr/asclepios/software/
MedINRIA). Regions of interest (ROI) were selected according to
FA maps. First, we determined the image with the highest FA value
of the cerebral peduncle in the axial plane FA maps. Then a 3×3
voxelsROIwasplacedinthecerebralpeduncletoproducethehigh-
est average FA value (Fig. 1). The number of fibers through the ROI
was calculated using the software. The FA threshold value was 0.20
to keep tracking based on the connectivity of the neighborhood.
0304-3940/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.neulet.2010.09.005

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B. Fu et al. / Neuroscience Letters 486 (2010) 132–135
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Fig. 1. Selection of the ROI in FA map. Angiography demonstrates a case of arteriovenous malformation (AVM) in the left parieto-occipital lobe (on the left). Region of interest
(ROI) (in red) is placed in the cerebral peduncles in fractional anisotropy (FA) map (on the right). The FA was 0.798 in the ipsilateral cerebral peduncle and 0.799 in the
contralateral cerebral peduncle.
All data are presented as means±SD and compared using t test.
Differences were considered statistically significant at a P value
<0.05.
In the AVM group, the complaints were epilepsy (11 cases),
headache (8 cases) and neurological deficit (5 cases). In the CM
group, the complaints included neurological deficit (7 cases),
headache (3 cases), epilepsy (3 cases) and asymptomatic (1 case).
In the tumor (glioma and meningioma) group, patients exhib-
ited neurological deficit (6 cases), headache (4 cases), epilepsy
(4 cases) and asymptomatic (1 case). The maximum diameter of
lesions was 33.9±11.3mm (range: 18–55mm) in the AVM group,
32.2±11.2mm (14–60mm) in the CM group and 40.9±15.3mm
(22–67mm) in the tumor group.
In the AVM group, there was no statistically difference between
mean FA of the ipsilateral cerebral peduncle (0.758±0.055)
and that of the contralateral cerebral peduncle (0.755±0.049)
(P>0.05). In the tumor group, mean FA was 0.713±0.084 of the
ipsilateral cerebral peduncle and 0.751±0.052 of the contralateral
cerebral peduncle (P>0.05). In the CM group, the FA measured in
the ipsilateral cerebral peduncle (0.711±0.092) was significantly
(P<0.01)lowerascomparedwiththecontralateralcerebralpedun-
cle (0.768±0.043). A significant reduction was also observed in the
ipsilateral FA of non-AVM lesions (the CM group and the tumor
group)ascomparedtothatofAVM(P<0.05).Buttherewerenosta-
tisticallydifferencesinthecontralateralFAbetweengroups(Fig.2).
The potential effects of age, sex, side and lesion location
on the DTI measurements were also investigated. All patients
(mean age 38.1±11.9 years, n=51) were divided into four groups
according to their age (<31 years, 31–40 years, 41–50 years, and
>50 years). Mean FA of the contralateral cerebral peduncle was
0.771±0.044 (n=14), 0.744±0.049 (n=19), 0.771±0.042 (n=8)
and 0.752±0.055 (n=10), respectively. There was no significant
difference between groups (P>0.05). The mean FA of the con-
tralateral cerebral peduncle was 0.760±0.043 in male (n=34)
and 0.752±0.057 in female (n=17) without statistically difference
(P>0.05). Whether the side was the left (0.753±0.050, n=30) or
the right (0.763±0.045, n=21) did not affect the FA value of the
contralateral cerebral peduncle (Fig. 3). There were 8 cases of AVM
and4casesofCMthatinvolvedtemporallobe.TheFAofthecerebral
pedunclewas0.786±0.048onipsilateralsideand0.744±0.056on
contralateral side in the temporal lobe AVM group. In the temporal
lobe CM group, FA was 0.727±0.022 and 0.770±0.015, respec-
tively. There was significant difference between bilateral side in
the temporal lobe CM (P<0.05), but not in the temporal lobe AVM
(P>0.05).Bycomparingtheresultsofipsilateralside,thedifference
between the temporal lobe AVM and CM was statistically signifi-
cant (P<0.05). No contralateral side difference was found between
(P>0.05) the temporal lobe AVM and CM (Fig. 3).
In the AVM group, the number of fibers through the ROI was
319.6±82.9 on ipsilateral side and 304.7±89.1 on contralateral
side (P>0.05). In the CM group, fiber number of ipsilateral side
(251±82.1) was significantly lower than that of contralateral side
(307.3±77.0) (P<0.05). In tumor, fiber number was 308.9±112.4
and 287.9±62.4 without significant difference between bilateral
side (P>0.05) (Fig. 4).
In literatures, DTI had been used in the evaluation of AVM
surgery and radiotherapy. DTI could demonstrate the relationship
of nerve tracts with AVM [12,17,33]. Some nerve tracts were less
Fig. 2. FA of the cerebral peduncle in the AVM, cavernous malformation (CM)
and tumor group. In the AVM group, FA of the cerebral peduncle is 0.758±0.055
on ipsilateral side and 0.755±0.049 on contralateral side. In the CM group, FA
is 0.711±0.092 and 0.768±0.043. In the tumor group, FA is 0.713±0.084 and
0.751±0.052. There is significantly difference between bilateral side in the CM
group (P<0.01), but not in AVM or tumor (P>0.05).

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B. Fu et al. / Neuroscience Letters 486 (2010) 132–135
Fig. 3. FA of the temporal lobe AVM and CM. The mean FA of the temporal lobe AVM
group is 0.786±0.048 on ipsilateral side and 0.744±0.056 on contralateral side. In
the CM group, FA is 0.727±0.022 and 0.770±0.015. There is significant difference
between bilateral side in CM (P<0.05), but not in AVM (P>0.05). By comparing
the results of ispilateral side, there is significant difference between CM and AVM
(P<0.05). No difference exists on contralateral side between CM and AVM (P>0.05).
visualized in patients with neurological symptoms than in asymp-
tomatic AVM patients [5,23]. The tolerant dosage of radiotherapy
varied in white matter [20–22]. It was DTI-guided navigation com-
bined with other techniques that made AVM removal safer [4,13].
Influence of age on FA had been reported. FA increased in pyra-
midal tract and corpus callosum not only in fetuses [6] but also in
healthy neonates [8]. In adult, age had significant negative correla-
tion with FA in the genu, rostral body and isthmus [24]. However,
the difference among the contralateral cerebral peduncle was not
statistically significant in this series, which was consistent with
the findings in healthy volunteers [34]. Another explanation was
relatively small subject number in our study.
The decrease in FA was reported in Wallerian degeneration,
which might be caused by infarction [19,29,35], cervical spinal
cord injury [10] and neurodegenerative disease [14]. Intracranial
hemorrhage [16], trauma [27], chronic subdural hemorrhage [34]
and subtotal hemispherectomy [32] had been associated with the
decrease in FA of the affected pyramidal tract.
It had been reported that the brain was able to compensate
for the functional deficits, that is, brain plasticity, which could
be revealed by fMRI. In 1999, Kombos et al. [15] reported a case
Fig. 4. Number of fibers through the ROI in the AVM, cavernous malformation (CM)
and tumor group. In AVM, fiber number of the cerebral peduncle is 319.6±82.9 on
ipsilateral side and 304.7±89.1 on contralateral side. In CM, number is 251±82.1
and 307.3±77.0. In tumor, number is 308.9±112.4 and 287.9±62.4. There is sig-
nificantly difference between bilateral side in the CM group (P<0.05), but not in
AVM or tumor (P>0.05).
of AVM with shift of motor region. Alkadhi et al. [1] found that
cerebral AVM led to reorganization within the somatotopic rep-
resentation in cortex and to occasional abnormal expansion into
nonprimary motor areas. Odzdoba et al. [25] reported abnormal
cortical activation patterns in AVM and shifts in the activation pat-
tern after endovascular procedures. Even language network shift
had been reported in stroke and AVM patients. Guzzetta et al. [11]
found in left perinatal stroke patients had extraordinary organi-
zational language capabilities. Vikingstad et al. [31] reported the
right hemisphere-shifted language network in the AVM group. The
reliabilityoffMRIintheAVMhadbeenquestioned,forthehemody-
namic perturbations in AVMs might impede the fMRI signal, such
as in perilesional eloquent cortex [30] and language reorganization
[18].ButThickbroometal.[28]reportedthefMRIsignalmagnitude
was not significantly affected in AVM.
The plasticity of white matter had also been reported. In the
multiple sclerosis patients, there were a significantly larger num-
ber of connections between the left and right thalami than in the
control subjects [2]. Ramu et al. [26] had discovered the brain fiber
tract plasticity in experimental spinal cord injury.
Our results show the ipsilateral FA of the cerebral peduncle
appears to be less influenced in AVM than in CM and tumor. And
thisdifferencewasnotassociatedwithage,sex,sideandlocationof
lesion. The findings indicated that possible plasticity of fiber tracts,
which might be secondary to cortical plasticity in AVM as demon-
strated by fMRI. And white matter plasticity differed in AVM, CM
and tumor, as showed by difference in FA value and fiber num-
ber in every group. It could be partly explained by our findings
that most patients with congenital AVM were asymptomatic until
adults.
There was the partial volume effect in DTI and heterogeneity in
eachgroup.Itwasreasonablethatthesmallervoxelsizewouldpro-
videmoredetailedinformation.Giventhesmallnumberofsubjects
reported in this preliminary study, future research should assess
the findings in a larger group of patients with smaller voxel size
and more homogeneity in groups.
The results from this study demonstrate that FA value and fiber
number of the cerebral peduncle is less affected in AVM than in
non-AVM lesions. The lack of the cerebral peduncle involvement
revealed by DTI indicates plasticity of white matter in AVM, which
is in keeping with observations from studies of the plasticity of
cortex in AVM by fMRI.
Acknowledgements
ThisresearchwassupportedbyagrantfromtheNationalNature
ScienceFoundationofChina(no.30830101).TheauthorsthankB.D.
Zhang(fromSiemensShenzhen)fortechnicalassistanceduringDTI
collection.
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