Analysis of the cervical double
transverse foramen in present
Spanish population
ORIGINAL ARTICLE Eur. J. Anat. 20 (4): 337-346 (2016)
Laura Quiles-Guiñau1, Azucena Gomez-Cabrero2, Marcos Miquel-Feucht1,
Esther Blanco-Pérez3, Federico Mata-Escolano4, Juan A. Sanchis-Gimeno1
1Department of Human Anatomy and Embryology, School of Medicine, University of Valencia, Valencia, Spain,
2Department of Hematology and Oncology, Children’s Hospital Los Angeles, Los Angeles, USA, 3Department of
Radiology, University Hospital de La Ribera, Alzira, Spain, 4CT and MRI Unit ERESA, Department of Radiology,
General University Hospital of Valencia, Valencia, Spain
SUMMARY
The aim of our study was to investigate the
prevalence and morphometry of double transverse
foramina in cervical vertebrae in a living population
and to discuss their clinical importance. This is
a retrospective single-center study. 253 (84.3%)
computed tomography scan images of the cervical
spine were collected from a total sample of 300
Spanish subjects that underwent a computed tomography
study, 173 from men (68.3%) and 80
from women (31.6%), aged between 18 and 90
years old. The presence or absence of a double
transverse foramen of each cervical vertebra was
recorded, and the maximum right-left diameter,
maximum antero-posterior diameter and area of
each transverse foramen were measured. The
applied statistics were multivariate models for repeated
measures, Student t test and Pearson’s chi
-squared test.
Double transverse foramina in C4, C5, C6 and
C7 were observed, the most prevalent being in
C6 (45.8%), followed by C5 (23.5%), C4 (4.7%)
and C7 (4.3%). The unilateral formation was
significantly the most frequent. No differences
were found based on sex. In the vertebrae with a
double transverse foramen, the principal transverse
foramen was significantly larger than the
accessory transverse foramen. However, in these
vertebrae the principal transverse foramen was
significantly smaller when compared with the
transverse foramen of normal vertebrae.
C6 presents the greatest prevalence of double
transverse foramina, although they are also observed
in C4, C5 and C7. The double transverse
foramen causes the principal transverse foramen
to be smaller when compared with normal vertebrae,
thus it should be taken into account in clinical
practice.
Key words: Anatomy – Skeleton – Spine – Computed
tomography – Spain
INTRODUCTION
The cervical spine presents biomechanical and
anatomical differences in comparison with dorsal
and lumbar vertebrae. One of the differences is the
presence of a transverse foramen (TF) in the
transverse process of cervical vertebrae, through
which the vertebral artery and veins and sympathetic
nerves pass, with the exception of the TF in
C7 which the vertebral artery does not pass
through (Jovanovic, 1990) (Fig. 1A).
The vertebral arteries are composed of four
segments (Fig. 1B and Fig. 1C). Segment V1,
the extra-osseous segment, goes from the beginning
of the vertebral artery until the transverse
foramen of the C6. Segment V2 is the foraminal
337
Submitted: 27 April, 2016. Accepted: 13 July, 2016.
Corresponding author: Laura Quiles Guiñau. School of Medicine,
University of Valencia, Dept. of Anatomy and Human Embryology,
Avda. Blasco Ibáñez, 15, 46010 Valencia, Spain.
Phone: 606 914 539. E-mail: laura.quiles@uv.es
Analysis of double transverse foramen
338
segment, where the artery passes through the
transverse foramina from C6 to C2. The extraspinal
segment, V3, begins at the foramen transversarium
of C2. At this segment, the vertebral
artery passes along the superior aspect of the posterior
ring of C1, and then twists antero-superior
towards the foramen magnum where it pierces the
dura. Lastly, V4, the intradural segment, courses to
the pontomedullary junction, where the basilar artery
is formed (Desouza et al., 2011).
Moreover, the cervical spine is the segment with
the most mobility of the spine. Therefore the relevant
clinical implications of the TF are obvious in
cases of possible compression or trauma of structures
that cross it, especially in relation to the vertebral
artery, depending on whether or not it affects
normal blood flow (Taitz et al., 1978). In this
context, variations in TF number and size are involved
in the etiology of some clinical syndromes
and symptoms like headache, migraine, fainting,
vertebrobasilar insufficiency as a response to certain
neck movements, and blackouts due to low
blood pressure in the vertebral artery (Bulsara et
al., 2006).
The TF can be multiple or absent and may present
anatomical variations with respect to its
shape and size. When it is multiple, the accessory
TF (ATF) usually appears posterior to, and
smaller than, the primary foramen (PTF) (Kaya
et al., 2011). This anatomical variant, called
double transverse foramen (DTF), has been
found in the inferior cervical rachis, either unilaterally
or bilaterally, and located more often in C6
(Murlimanju et al., 2011; Chandravadiya et al.,
2013). In terms of its etiology, DTF may be related
to variations of the course and development
of the vertebral artery (Das et al., 2005). In addition,
it is fundamental to understand the anatomic
variations of the TF in order to properly
plan surgical procedures of the cervical spine
including screw fixation, since the osseous and
vascular variations of the cervical spine can
place the vertebral artery at risk during surgery
(Peng et al., 2009).
We hypothesize that there were morphometric
differences between the PTF, the ATF and the
normal TF at all the cervical levels presenting DTF.
Following on from this, the aim of our study
was to investigate the quantitative anatomy
and morphometry of TF with emphasis on the
prevalence of DTF in order to increase and consolidate
the current anatomic knowledge, as the
TF is fundamental for surgical treatment of vertebral
artery dissection and laceration.
MATERIALS AND METHODS
Patient sample
This was a morphologically based, retrospectively
designed and single-center study. It was approved
by the Ethics Committee in Human Research
of the University of Valencia (ref.
H1414410627187). The procedures were performed
in accordance with the World Medical
Association Declaration of Helsinki (1975 and
subsequent additions).
We reviewed computed tomography (CT) cervical
scans of 300 consecutive Spaniard subjects
aged between 18 and 90 years old. CT studies
were carried out at the CT ERESA Unit at the
University General Hospital of Valencia, Spain.
The CT scans were reviewed by two different radiologists.
Only when both radiologists coincided in
the diagnosis the CT images were used for the
study.
Inclusion criteria were Spanish subjects aged
more than 18 years that underwent a CT study.
The exclusion criteria were: incomplete studies
(when the complete cervical spine was not included),
metal artifact imaging, previous cervical
spine surgery, trauma or vertebral fractures, tumor
history or cervical spine infections, severe rheumatic
disease, myelopathies and congenital cervical
malformations, as well as those related to
Down Syndrome, Turner Syndrome, Arnold-Chiari
malformation, Klippel-Feil Syndrome, and other
Fig. 1. Scheme of the vertebral arteries in the cervical
vertebrae TF. (A) Transversal view of a typical cervical
vertebra showing the vertebral artery and veins passing
through the TF. (B) Lateral view of cervical spine
and vertebral artery. (C) Anterior view of cervical spine
and vertebral arteries. The vertebral artery is composed
of 4 segments: V1 begins at the origin on the
subclavian artery and extends to the C6 TF; V2 runs
from the C6 TF to the C2 TF; V3 extends from the
C2 TF to the foramen magnum; V4 runs from the foramen
magnum to the vertebrobasilar junction.
L. Quiles-Guiñau et al.
339
congenital malformation syndromes.
In accordance with our inclusion and exclusion
criteria, 253 (84.3%) CT scan images of the cervical
spine were collected from a total sample of
300 Spanish subjects (100%), 173 men (68.3%)
and 80 women (31.6%). Table 1 shows the number
of images that were analyzed at each cervical
level as well as the number of images that were
discarded because there was no coincidence between
radiologists.
The mean overall age of the study sample
was 63.5 ± 13.0 years old. The mean age of
the men (64.7 ± 11.2 years old) was slightly
higher than that of the women (60.9 ± 16.1 years
old) and this difference was statistically significant
(Student t test p = 0.033). The main reason for
performing the CT scans that were analyzed in
this study was internal carotid artery diseases
(82.6%), followed by other vascular diseases that
did not affect the vertebral artery (10.6%), certain
types of neoplasms (4.4%), and cerebrovascular
diseases (2.4%).
CT scan protocol
All the image studies were performed with a GE
LightSpeed VCT 64 Slice CT system (General
Electric, Milwaukee, WI, USA) providing an axial-
field of view of 350-400 mm and a trans-axial
slice thickness of 0.5 mm. A low-dose CT scan
from the aortic arch through the orbitomeatal baseline
was obtained with the patient in the supine
position (120Kvp, 300mAs, 0.5-s rotation time,
16x0.5mm collimation, pitch of 0.64).
An 18 to 20 gauge angiocath was inserted into
the antecubital vein of all the patients. Over 70–
120 ml of non-ionic iodinated contrast media
(iopamidol 300) followed by 30 ml of saline solution
was injected with an automatic injector at a
rate of 5 ml/sec. The bolus-tracking method proved
very useful for correct filling of the vertebral arteries.
The region of interest was positioned at the
aortic arch, and the threshold was set at 100-
120 HU; when it was surpassed, helical scanning
was automatically initiated.
Morphometric parameters
Images were analyzed on a GE Advantage
Windows 4.5 workstation. Three measurements
for each TF of all cervical vertebrae were obtained
using screen images: its width (maximum right-left
diameter) its depth (maximum antero-posterior
diameter) and its area were recorded. The larger
TF was deemed the principal (PTF) in the vertebrae
with a DTF, while the smaller and accessory
of the two foramina was deemed the ATF. Fig. 2
shows an example of a dry C6 vertebra with bilateral
DTF, and Fig. 3 shows CT scan images of
C4, C5 and C6 vertebrae with unilateral DTF.
Statistical analyses
The descriptive statistics were calculated to
define the sample. Multivariate models for repeated
measures were used to adjust for uncertain
variables like age and sex. Student t test was
used to estimate the differences of the means between
two independent groups. Pearson’s chisquared
test was used to compare the distributions
of the frequencies. A p value of ≤ 0.05 was considered
significant. Continuous variables are
showed as average and standard deviation of the
mean. Category variables are shown as frequencies.
The statistical analyses were performed with
SPSS ver.13 statistical software package (SPSS
Inc., Chicago, IL, USA).
RESULTS
After adjustment for uncertain variables like sex
and age, there were no statistically significant differences
between men and women regarding the
presence of DTF: 7 C4 vertebrae (4.3%) with DTF
in men, and 4 (5.6%) in women (p = 0.453); 35 C5
vertebrae (21.7%) with DTF in men, and 20
(27.4%) in women (p = 0.217); 69 C6 vertebrae
(46.6%) with DTF in men, and 29 (43.9%) in women
(p = 0.415); 4 C7 vertebrae (2.8%) with DTF in
men, and 5 (7.6%) in women (p = 0.119).
The general prevalence of DTF in all the vertebrae
analyzed was 11.2%. The presence of DTF
Table 1. Number of CT scan images analyzed and number of CT scan images discarded by diagnosis disparity between
radiologists
Cervical level CT scan images analyzed CT scan images discarded
C1 226 (89.3%) 27 (10.6%)
C2 193 (76.2%) 60 (23.7%)
C3 233 (92.0%) 20 (7.9%)
C4 234 (92.4%) 19 (7.5%)
C5 234 (92.4%) 19 (7.5%)
C6 214 (84.5) 39 (15.4%)
C7 207 (81.8%) 46 (18.1%)
CT = computed tomography scan
Analysis of double transverse foramen
340
was more frequent in C6 (98 vertebrae, 45.8%),
followed by C5 (55 vertebrae, 23.5%), C4 (11 vertebrae,
4.7%) and C7 (9 vertebrae, 4.3%). Depending
on which side was the altered one, the
frequency of DTF by cervical level was as follows:
in C4, 7 (0.2%) on the right side, 3 (1.2%) on
the left side and 1 (0.4%) bilateral; in C5, 30
(12.8%) on the right side, 13 (5.5%) on the left side
and 12 (5.1%) bilateral; in C6, 35 (16.3%) on
the right side, 21 (9.8%) on the left side and
42 (19.6%) bilateral; and in C7, 6 (2.8%) on the
right side, 3 (1.4%) on the left side and 0 (0,0%)
bilateral. There was a statistically significant greater
prevalence of unilateral DTF than bilateral cases
in C4 (p=0.004), C5 (p=0.001) and C6
(p=0.001). In addition, there was a greater prevalence
of DTF on the right side at all four cervical
levels studied, although this difference was not
statistically significant (C4 p=0.476, C5 p=0.154,
C6 p=0.303, C7 p=0.453).
In the vertebrae presenting DTF (C4-C7) we observed
sexual differences in TF measurements.
The lateral diameter, antero-posterior diameter
and area of TF were bigger in men than in women.
This difference was statistically significant for
the antero-posterior diameter at C1, the lateral
diameter at C1-C6 and the area at C1, C3-C6
(Table 2).
The antero-posterior diameter, lateral diameter
and area of the PTF were larger than the ones of
the ATF in all the vertebrae with DTF, and these
differences were statistically significant at all the
cervical levels analyzed, except in the case of the
lateral diameter and area of the PTF of C7, in both
Fig. 2. Image of a dry C6 vertebra with bilateral DTF.
PTF: principal transverse foramen. ATF: accessory
transverse foramen.
Fig. 3. CT scan images of cervical vertebrae with
DTF. (A) C4 vertebra with a right DTF. (B) C5 vertebra
with a left DTF. (C) C6 vertebra with a left DTF.
men and women (Table 3).
As Table 4 shows, when comparing the dimensions
of the PTF in vertebrae presenting DTF
with the dimensions of the TF in vertebrae
without a DTF at the cervical levels C4, C5, C6
and C7, the presence of DTF determined a smaller
size of the PTF in comparison with the TF of normal
vertebrae. This difference was statistically significant
in both men and women (except for the
lateral diameter of C6 and C7 in men, and the lateral
diameter of C6 in women).
L. Quiles-Guiñau et al.
341
Table 2. Sexual differences in measurements of TF of normal cervical vertebrae
SD: Standard Deviation; 1 antero-posterior diameter (mm); 2 lateral diameter (mm); 3 area (mm2); 4 P-value in comparison between men and women
(Student t test)
Cervical level
Men Women
Media ± SD Range Media ± SD Range p4
C1 (♂=154, ♀=72)
Ø AP 1 7.1 ± 1.0 3.2 - 10.0 6.7 ± 1.0 3.8 - 9.6 0.001
Ø lat 2 5.9 ± 0.9 3.6 - 9.1 5.5 ± 0.8 3.7 - 7.8
0>
Analysis of the relationship between the double transverse foramen and the possibility of developing clinical symptoms after whiplash:
0>
ABSTRACT
Introduction: Currently there is no information about the possibility of developing clinical symptoms after whiplash in double transverse foramen subjects. Our aim was to test whether subjects with double transverse foramen have an increased risk of presenting with acute headache, dizziness, vertebral artery dissection, and vomiting after whiplash.
Methods: We recorded the absence/presence of double transverse foramen, and the absence/presence of neck pain, acute headache, dizziness, vertebral artery dissection, and vomiting in 85 patients who had suffered whiplash injuries in car rear-end impacts in road traffic accidents. We used the odds ratio test to determine whether double transverse foramen subjects are at a higher risk of developing acute headache, dizziness, and vomiting than non-double transverse foramen subjects.
Results: Although double transverse foramen subjects presented with more clinical symptoms after whiplash, the odds ratio test revealed that their risks of developing acute headache (p=0.30), dizziness (p = 0.09), or vomiting (p=0.18) were not significantly greater than in the control group.
Conclusions: Double transverse foramen subjects are not at a higher risk of presenting acute headache, dizziness, vertebral artery dissection, and vomiting after whiplash. This article is protected by copyright. All rights reserved.
http://ift.tt/2rmzjrw
Δεν υπάρχουν σχόλια:
Δημοσίευση σχολίου