Title : Posterior Basicranium asymmetry and idiopathic scoliosis
Authors :D. L. Rousie, Docteur en Neurosciences (1), O. Joly, PhD student (1), A. Berthoz,
Professeur au College de France (1), ( (1) Laboratoire de la perception et de l action, College
de France, Paris)
Name and adress for correspondence : Docteur Rousie, 3 rue Saint Louis, 59113 Seclin
France. Fax: 0033 320 32 35 44, Tel. 0033 320 90 12 29, firstname.lastname@example.org
Fondation Yves Cotrel pour la recherche en pathologie rachidienne. Institut de France, Paris.
SHFJ/CEA Orsay in the frame of the cooperation through IFR 49 INSERM/CNRS France.
Key points :
Posterior Basicranium (PBA), divided in 2 parts joined to the foramen magnum, presents a
torque in Idiopathic scoliosis (IS)
PBA torque reflects cerebellar asymmetry in IS.
PBA torque induces spatial asymmetry of the vestibular system and specially, of the otolithic
system, with potential consequences on vestibular function and posture in IS.
PBA asymmetry and idiopathic scoliosis
Are there neuro-anatomical abnormalities associated with idiopathic scoliosis (IS)?
Posterior Basicranium (PBA) reflects cerebellum growth and contains vestibular organs, two
structures suspected to be involved in scoliosis.
The aim of this study was to compare posterior basicranium asymmetry (PBA) in Idiopathic
scoliosis (IS) and normal subjects.
Method: To measure the shape of PBA in 3D, we defined an intra-cranial frame of reference
based on CNS and guided by embryology of the neural tube. Measurements concerned three
directions of space referred to a specific intra cranial referential. Data acquisition was
performed with T2 MRI (G.E. Excite 1.5T, mode Fiesta). We explored a scoliosis group of 76
women and 20 men with a mean age of 17, 2 and a control group of 26 women and 16 men,
with a mean age of 27, 7.
Results: IS revealed a significant asymmetry of PBA (Pr>|t|<.0001) in 3 directions of space
compared to the control group. This asymmetry was more pronounced in antero-posterior
(AP) & lateral direction, forming a torque of the posterior base shape associated with identical
Discussion: IS Cerebellar and PBA asymmetries are neurodevelopmental anomalies involved
in IS. The vestibular systems are embedded in the 2-parted PBA and, therefore, are in
asymmetrical spatial position with potential consequences on otolithic function because this
latter is devoted to gravity.
In 2002, Kwak demonstrated links between patterning of the cerebellum and alterations in the
development of the internal ear in experimental zebra fish (focused on semi-circular canals
formation) We engaged a study on IS semi-circular canals anatomy thanks to a novel program
of modelling. We will report our first results in the companion paper.
Pba asymmetry and idiopathic scoliosis
According to a report by Nachemson,idiopathic Scoliosis (IS) is now generally recognized
to be caused by several conditions: genetic, [2, 3], hormonal [4, 5], neuro-anatomical [6, 7, 8]
and/or neuro-muscular [9, 10].
Various studies have reported links between IS and asymmetry at similar functional and
anatomical levels: Chockalingam , Shimode, Kramersand Perret have
reported right/left asymmetries at functional levels for gait or motor control parameters.
Geissele  and Kertesz have stressed the presence of links between IS and right/left
brain asymmetries. Geschwind & Galaburda  have highlighted asymmetries of the
temporal planum, with the left planum being more developed in 65% of examined brains.
In a study by Lundstrom  60 to75% of the examinated population has a left hemisphere
larger than the right. He measured the angle formed by a line drawn from the ear to the
median line. This anatomical detail has also been noted by Burke  who pointed out that
cause of this asymmetry is still unknown. More recently, neuro-anatomical abnormalities in
the pontine and hindbrain regions have been clearly implicated, in IS, in a report by Lowe
 in 2000.
Pirttiniemi, Lahtela, Hunggare & Serlo, Delaire, Berthoz &Rousié [22,23] have
reported the presence of craniofacial asymmetry(CFA) in certain cases of scoliosis and /or
laterocolis. These asymmetries are associated with spatial asymmetries of vestibular organs
involved in postural control.
CFA implicates asymmetry of each bony component of the head: vault, face and basicranium.
The basicranium is divided in three parts: the anterior part, the middle part which is a true
patella which makes the 3D movements of the two other parts possible and the posterior part
in which the labyrinths are embedded.
The basicranium shape reflects the underlying brain growth. Cerebral asymmetry appears, in
utero,at the beginning of the third week. At this stage, the basicranium is a pre-cartilaginous
and flexible structure: the three parts of the base are separated by large and mesenchymal
synchondrosis avoiding any pressure that could affect the brain growth [24, 25]. It is therefore
obvious that no basicranium asymmetry would occur without cerebral asymmetry.
The aim of this study was to compare the shape of the posterior basicranium (PBA) on IS and
non-IS subjects. This study was conducted for two reasons: 1) the PBA reflects the growth of
the cerebellum, the asymmetry of which is though to be implicated in scoliosis [19, 26] and 2)
the PBA contains vestibular organs implicated in postural disorders .
Materials and Methods
MRI acquisition and measurement of basicranium asymmetries
Data, in all MRI machines are included in a volume, which is itself included in the reference
frame of the machine. Three dimensional-coordinates of a selected point (voxel) are
calculated from this frame and are dependent on the patient‟s head orientation in the machine.
Precise measurements require a reliable frame of reference, apart from the patient head
orientation during the acquisition. These measurements should allow comparison of the
spatial location of head paired structures in a subject but also between different subjects.
We used an intra-cranial frame of reference based on the central nervous system .
We assigned our reference points on the basis of embryology: the neural tube stage marks the
beginning of the cranio-caudal orientation of the embryo especially at the cerebral level. This
stage is also the epicenter of brain-lobes growth and at this stage, asymmetry is not yet
The neuro sagittal medial plan (NSM), (red plan in Figure 1)-is built from points located on
the axis upon which this embryonic neural tube was fastened: two points are taken
successively along on the fundus of the third-ventricle (mesencephalon) and one point is taken
at the level of the cerebral aqueduct joining the third to the fourth ventricle (see Figure 2A, B,
The axial plan-(blue plan in Figure 1)- is perpendicular to NSM plan and goes through the CA
(anterior commissure)-to CP (posterior commissure) axis which provides the principal point
of reference in Talairach‟s atlas . Thus, to build this plan, we used the three following
points: CA, CP and the point where CA-CP axis crosses the sagittal plan.
The frontal plan-(green plan in Figure 1B) - is perpendicular to the previous ones.
After constructing this frame of reference; it became possible to compare the 3D location of
paired structures of the head.
The PBA is divided into two parts: the left and right petrous pyramids joined to the foramen
magnum. We used the junction between the auditory meatus and the three vestibular semi-
circular canals as markers to measure the spatial position of each part. These points, named P
(right) & P‟ (left)-and situated inside the PBA, are precise and easy to find. (See Figure
Data acquisition was performed with EXCITE MRI 1.5T., from General Electric,
using a head coil. A T2-weighted sequence was used in 3D FIESTA mode acquisition Thus,
PBA structures were analysed in a volume instead of classical MRI slices. The quality of data
was monitored by a G.E. work station 4.1 and stored on a CD.
We processed the data using various modules of Brainvisa which is free access software
devoted to MRI available on the web (http://brainvisa.info/).
Various steps of the process:
1-Import and convert MRI data (Dicom format) given by the GE machine to „Gis
Brain visa‟ format.
2- Select and save points needed for the construction of the reference frame. For each
chosen point, a module of Brainvisa called Anatomist 1.3 provides 3D coordinates referenced
to the reference frame of the MRI machine.
3- Select and save the markers points P (right) and P‟ (left).
4- Plans and distances :we automated the following procedure in a novel program in
order to measure the 3D location of P&P ‟referenced on our reference frame: in a
mathematical method, we calculate the equation of the planes using Cartesian coordinates of
three distinct points : A(xA, yA ,zA), B(xB,yB,zB) et C(xC,yC,zC)
The equation of plan is: ax + bx+ cz +d=0. The program automatically calculates the
distances of these three points to the plans.
By measuring the distance differences between P and P‟-to each of the 3 planes, we can
define the spatial orientation of both parts of the PBA:
1) to the NSM plane = dP_sag – dP‟_sag, 2)to axial plane =dP_axial – dP‟_axial, 3) to the
frontal plane = dP_front – dP‟front. These distances are given in millimeters.
We used a similar procedure for each patient for establishing inter-patients comparisons.
Pba asymmetry and idiopathic scoliosis
Patients and control subjects
No data was available in relation to PBA evaluation in IS patient at the time of the planning:
thus the sample size could not be estimated before hand. The number of IS patients was fixed
between 80 and 100 because some abnormalities may be uncommon in the studied IS
population and also because classical statistical analyses related to categorical variables
require such sample size. The number of controls was kept to 30 as the Student‟s t-test has
been shown to be robust when the sample size is not too small.
a) Control group (CG)
Justifying a MRI for healthy individuals was difficult: thus, control subjects were recruited
from patients undergoing maxillo-facial consultation and suffering from lesions of the
temporomandibular joints which are similar to our regions of interest. These lesions do not
interfere with spine or PBA and these patients can be included as normal control subjects. We
exploited, their MRI results, which have been carried through in the context of their
therapeutic treatment. The criteria for inclusion were strictly observed: patients were required
to be free of any spine deformation, whether congenital or acquired which was confirmed by
the rheumatologists of our team. All of these subjects were consenting to give their MRI and
spine data (spine radiographies) in an anonymous way for the study.
This control group (CG) included 33 persons, 27 women and16 men, ranging in age from 8 to
51 years with a mean age of 27, 7 years (std. dev: 5.6).
106b) Scoliosis group (SG)
For the scoliotic group (SC), the exclusion criteria were to be free of acquired or congenital
spine lesion, of visual or auditive malformation which could have postural incidences and of
systemic illness. IS patients have been recruited from patients treated by physiotherapy and/or
brace by rheumatologists of our team (hospital or clinics). The recruitment was time-
randomized (23months): patients, presenting the inclusion criteria, were asked to participate
to the study as they came along to consultations. MRI was prescribed, in the course of their
therapeutic treatment to control malformations or lesions in the skull base or cervical spine
(which could also be exclusion criteria).They gave their consent to give their MRI and spine
data, in anonymous way, for the study.
SG included 95 patients, 75 females and 20 males, ranging in age from 10 to 30 with a mean
age of 17.3 (Std. dev.: 4.7).The greater number of females reflects the well-known large
incidence of idiopathic scoliosis on female.
Their scoliosis was classified following two criteria
1 –Cobb angle: two sub-groups were distinguished according to the severity of the
curve: SG1: from 12 to 20 degrees, including 57 subjects with a mean age of 14, 8(std. dev.:
3.01). SG2: from 20 to 47degrees including 38 subjects with a mean age of 18, 9(std.dev. 3,
2- Location of the deformation along the spine according to the Cottalorda and Kohler
The randomized recruitment, spread over 23 months, allowed us to divide the same 95
patients in three sub-groups:
- 57 patients with a thoracolumbar deformation formed the TL subgroup (52 with left TL and
5 with right TL)
- 24 patients with a thoracic deformation formed the T subgroup (22 with right T and 2 with
- 14 patients with a lumbar deformation formed the L subgroup (13 with left L and 1 with
We evaluated the reliability of our method by testing the reproducibility of our results with
test-retest correlation (RO-intra) using the Fermanian Intra-class correlation reported by Fleiss
. The Fermanian scale of evaluation is as follows: RO>0.91= very good;
0.71<RO<0.91=good; 0.51<RO<0.71= moderated.
We measured the dP-dP‟distances to the NSM, frontal and vertical planes.
As recommended in the method, these measurements were carried out three times. Thus, for
each subject, we collected nine measurements. This evaluation was carried out using 26
We obtained the following results:
To the NSM, RO=0.97752 with an inferior limit=0.94739, sup. Limit=0, 99048; Estimation=
To the frontal plane RO=0, 97872, inferior limit=0, 95014, sup. Limit=0, 99099;
To the vertical plane RO= 0, 93930, inferior limit=0, 86152, sup. Limit= 0, 97401;
Estimation= very good.
All statistical analysis was performed by means of SAS software (SAS Institute Inc.
Cary, NC 25513). P values<0.05 were considered statistically significant. Results were
expressed as the mean, standard deviation and range .The assumption of equal variances was
tested using the Fisher‟s test. The student‟s test was used because this assumption was not
Comparison between normal and scoliosis Basicranium asymmetries
IS patients (SG) presented significantly greater asymmetry of the PBA orientation in 3
directions of space than the control group (CG)
-Frontal plane: in SG, dP-dP‟ (mean value) = 5,662mm, Pr>|t|<.0001;
in CG, dP-dP‟ (mean value) = 2,140mm, Pr>|t|<.0001
-NSM plane: in SG, dP-dP‟ (mean value) = 3,573mm, Pr>|t|<.0001
in CG, dP-dP‟ (mean value) = 1,945mm, Pr>|t|<.0001
-Vertical plane: in SG, dP-dP‟ (mean value) =3,516mm, Pr>|t|<.0001
in CG, dP-dP‟ (mean value) =1,264mm, Pr>|t|<.0001.
We determined the right /left asymmetry of the 2-parted PBA, by establishing the
following differences: dP- dP‟negative, in relation to the NSM plane, meant that P was closer
than P‟. dP- dP‟ negative in relation to the horizontal plane, meant that the P was lower and
dP-dP‟ negative, in relation to the frontal plane, meant that P was backward. Measurements
were only calculated for the SG group.
We found: the right part of the PBA referenced to the frontal plane, backward in 66/95(69,
4%). The right part of the PBA referenced to the NSM plane was laterally closer than the left
one in 54/95(56, 8%). And, referenced to the horizontal plane, the right part was lower than
the left one in 73/95(76, 8%). Indirectly, this PBA torque suggested that underlying
cerebellum was, most of the time, larger on left side.
The purpose of this study was to verify the association between scoliosis and PBA.
Our first result was methodological in which we proposed a novel technique for analyzing
scoliosis: an intracranial frame of reference built from the NSM plane, automated in a
programme for identifying the asymmetry proved to be a reliable tool due to statistical
analysis. This technique may be useful for diagnosis in radiology but also for fundamental
studies in development.
The relation between scoliosis and posterior basicranium asymmetries
Our second result was in relation to our suggestion that scoliosis patients, in
comparison with normal subjects are afflicted with a significant asymmetry of the posterior
basicranium(figure 4). Interestingly, even with non-scoliotic control subjects, this part of the
base shows weak asymmetry which is consistent with other studies of brain and skull
asymmetries [32, 33] Coffin , reported similar observations in 1986, and speculated that
this asymmetry might have started during the first three months; this is because at this stage,
the basicranium is still flexible and open to changes in its shape depending on brain growth.
The “normal pattern” we obtained, provides the limits for normality and a preliminary scale of
comparison. However, it would be necessary to increase the number of subjects to refine the
pattern exhibited by our study with other similar groups.
IS versus control subjects revealed a significant antero-posterior and weak dorso-
ventral movement of the posterior base following asymmetrical brain growth.
Our results were also in accord those of Villemann (1976)  who confirmed that impact of
neural mass growth can modify the spatial orientation of the basicranium; In our study, we
highlighted that the two aisles of PBA form a torque around the foramen magnum. Recent
MRI scans confirm our findings: in 2006, Lancefield  found that brain torque may be
observed in the latter part of foetal life. IS patients show an exaggeration of this torque.
Similarly, Lacy and Horner (1996) have also demonstrated that “asymmetry” can be
considered as a threshold phenomenon in cases of genetic and /or environmental
modifications: they observed that skull and skeletal asymmetries increased with genetic
transmission in the last few populations of rats that have been maintained under abnormal
living conditions . Morever, Lowe  has suggested a possible implication of the
midbrain or hindbrain in IS. The cerebellar torque we found is also associated with an
asymmetry between the right and left part of the cerebellum. A question remains whether the
cerebellum asymmetry could be involved through its spatial organisation or its cortical
function. Further studies could be engaged.
In the method we differentiated IS group in SG1 and SG2 subgroups for a better
presentation of IS patients. One could wonder if the severity of the spine deformation is
related to the amplitude of the PBA torque. We did not lead this comparison because, in the
course of the study, we discovered a bias between these two subgroups: the mean age of the
patients in SG1 and SG2 was, respectively, 14.8 and 18.9. In SG1, patients were younger and
IS were still progressive forbidding the comparison. We should lead linear study to shed some
light on this question.
Pba asymmetry and idiopathic scoliosis
This study linked face asymmetry to basicranium asymmetry: temporo-mandibular joints
hang the mandible to the posterior basicranium. This is expressed on the face and can easily
be verify visually by simply assessing the implantation of the IS patient‟s ears and eyes during
the clinical examination of the face. At the bones level of the face, PBA frequently,induces
asymmetry in orbits location, deviation of the nasal septum, jaw and zygomatic arch
asymmetry. This observation was previously reported by Burke 1992 Chebib and
Chamma 1981, Lundstrom 1961 and especially Previc in 1991  who carried out
an extensive study of cranio-facial asymmetries confirming the association between scoliosis
and cephalic asymmetry – although without making use of any other comparative methods.
The second part of our study on the PBA concentrated on the vestibular system which
is widely though to be implicated in IS. The asymmetrical spatialization of the PBA aisles in
which the labyrinths are embedded, suggests functional consequences as a result on vestibular
function. The otolithic system which is a gravity devoted system could be responsible for
passing asymmetrical information to the postural system. Previc (1991) (40),Bacsi (2004)(27)
have stressed the contribution of vestibular asymmetry in postural disorders and on the
asymmetry of the vestibulospinal reflex. Recently, Burwell (2006)  suggested that
neurodevelopmental anomalies were implicated in CNS body schema and may be the primary
in of idiopathic scoliosis. We are currently studying IS otolithic function
IS cerebellum and PBA asymmetries are neurodevelopmental anomalies. In 2002,
Kwak showed with zebra fish that the experimental „Valentino‟mutation disturbed the
patterning of the cerebellum with, as a secondary consequence, alterations in the development
of the internal ear due to poor expression of the fibroblastic factor fgf3. In 2004, Philips 
confirmed the implication of factors fgf3 and fgf8 in the formation of the cerebellum and otic
placodes. More, Riley in 2003, has discovered that cells abutting the posterior lateral
hindbrain coordinates the early patterning of the inner ear giving to the fore the close relation
between the hindbrain and the vestibular system 
The fact that fibroblastic factors figure equally in the formation of inner ear,
cerebellum and Base suggests an identical co-involvement, in IS. We therefore designed a
novel method for visualizing the anatomy of the vestibular system and more precisely that of
the membranous semi-circular canals. The first results will be published in a compagnon
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Titles & legends of figures
Figure 1 the intracranial frame of reference
View of the referential included in a 3D reconstruction of the head. With this referential the
measurements are independent of the head‟s patient orientation during MRI and it allows
inter-subjects PBA comparisons.
Red plane=sagittal plane used for lateral measurements, blue plane= axial plane used for
vertical measurements, green plane= frontal plane used for anteroposterior measurements
Figure 2 : A Axial view
The fundus of the third ventricle is easily identified on this axial view. The crossing lines
point corresponds to the first selected point located on the third ventricle. Its 3D coordinates
are automatically transmitted to the programme.
Figure 2B : Medial-sagittal view
On this medial-sagittal view the same selected point appears on the fundus of the third
ventricle. This view permits to control the validity of our selected point.
Figure 2C & 2D : Medial-sagittal view and selected points
These two views show the two others selected points which are required to create the medial
axial plane of the referential.
Figure 3A & 3B : Selection of P& P‟ points
The junction between the auditory meatus and the three vestibular semi-circular canals are
selected as markers to measure the spatial orientation of the two PBA petrous parts. The black
arrows indicate these junctions, named P (right) (3B) & P‟ (left) (3A) situated inside the PBA.
They are precise and easy to find. The asymmetries of the cerebellum and PBA torque
deformation appear on these two axial views.
Figure 4 : Symmetrical PBA of a non-IS subject
This control subject presents a symmetrical PBA. The cerebellum is symmetrical. P&P‟ are
located on the same horizontal line.
Figure 5 : X-Rays Thoraco-lumbar scoliosis
This patient was the one afflicted with PBA asymmetry detailed in figure 3A & 3B. The
asymmetry was calculated with our programme: dP-dP‟= - 4. 32mm in relation to the frontal
plane, meant that P was backward (AP asymmetry); dP- dP‟= - 2.54mm in relation to the
NSM plane, meant that P was closer than P‟ and dP- dP‟= - 3,89mmin relation to the
horizontal plane, meant that the P was lower than P‟. These different results measure the
torque deformation of PBA.