Morphometric study of accessory foramen transversarium and their clinical importance

Full text

437
Drug Invention Today | Vol 11 • Issue 2 • 2019
Morphometric study of accessory foramen transversarium
and their clinical importance
R. Revathy1, Yuvaraj Maria Francis2*, S. Pavithra1, A. Priyadarshini2, Balaji Karunakarn2,
Gunapriya Raghunath2, K. Rekha1
INTRODUCTION
The vertebral column is a part of axial skeleton of
man which has to protect the spinal cord and support
the body. There are seven cervical vertebrae and are
identified by the presence of foramen in their transverse
processes called foramen transversarium - the cardinal
feature of cervical vertebrae. Of these seven, third to
six is typical and first, second, and seventh are atypical
cervical vertebrae. Typical cervical vertebrae consist
of two major parts, an anterior, cylindrically shaped
vertebral body and a posterior, irregularly shaped
neural arch. The body of the vertebrae is small, with
a transverse diameter greater than its anteroposterior
diameter in cervical vertebrae. To minimize the
Research Article
1Department of Physiotherapy, Saveetha College of Physiotherapy, Thandalam, Chennai, Tamil Nadu, India, 2Department of
Anatomy, Saveetha Medical College Hospital, Thandalam, Chennai, Tamil Nadu, India
*Corresponding author: Mr. Maria Francis Yuvaraj, Department of Anatomy, Saveetha Medical College Hospital, Thandalam,
Chennai, Tamil Nadu, India. Phone: 91-9952929636. E-mail: sujinalways@gmail.com
Received on: 13-11-2018; Revised on: 26-12-2018; Accepted on: 21-01-2019
Access this article online
Website: jprsolutions.info ISSN: 0975-7619
weight of the vertebrae and allow dynamic load
bearing, the vertebral body is not a solid block of bone
but a shell of cortical bone surrounding a cancellous
cavity. The cortical shell is reinforced by trabeculae in
the cancellous bone, which helps resist compressive
forces.
The neural arch can be further divided into the pedicles
and the posterior elements. The pedicle is short, stout
pillars with thick walls that transmit tension and
bending forces from the posterior elements to the
vertebral bodies. The remaining posterior elements are
the laminae, the spinous process, and the transverse
process. The spinous process is the posterior projection
of bone that originates from the central portion of the
lamina, dividing into two. The transverse processes
are lateral projections of bone that originates from
the lamina. It is made up of two elements transverse
element and costal element. The transverse element
fuses with the costal element and forms the medial part
ABSTRACT
Aim: To determine the presence of accessory foramen transversarium of cervical vertebrae and to investigate them according
to their size, shape, location, diameter, and their changes related to the vertebral artery and their clinical significance.
Material and Methods: The study was done in Saveetha Medical College, Thandalam, and 120 cervical vertebrae were
procured from the Department of Anatomy to find the presence of accessory foramen transversarium and investigate them
according to their morphometry based on size, shape, location, classification, and diameter. The size were measured by
digital vernier caliper. Results: Out of 120 cervical vertebrae, accessory foramen transversarium is found only in 39 cervical
vertebrae. Of these, 20 were complete and 19 were incomplete foramen. Based on shape, 11 round, 18 oval, and 10 irregular
shapes were seen. Unilaterally 28 and bilaterally 11 accessory foramen transversarium were found. About 28 accessory
foramen transversarium were seen in front and 11 were seen at the back in relation to foramen transversarium. Antero-
posterior and transverse diameter of 39 accessory foramen transversarium was measured and their mean and standard deviation
were calculated. Discussion: The neck is the part of long vertebral column which has cervical vertebrae. There are seven
cervical vertebrae and are identified by the presence of foramen in their transverse process called foramen transversarium,
the cardinal feature of cervical vertebrae. The knowledge of the dimension of both foramen transversarium and accessory
foramen transversarium may contribute as additional information for the clinical during any procedure around cervical
region. Conclusion: The knowledge of the presences of accessory foramen transversarium is important for radiologist and
clinicians during vascular surgeries and neurosurgeries.
KEY WORDS: Accessory foramen transversarium, Cardinal feature, Cervical vertebrae, Morphometry, Vertebral artery

R. Revathy, et al.
Drug Invention Today | Vol 11 • Issue 2 • 2019
438
of the posterior wall of the foramen transversarium.
The costal element has anterior and posterior roots
which end in anterior and posterior tubercles joined
together by costotransverse bar. The vertebral artery
is one of the two principal arteries which supply the
brain.[1] It branches from the first part of subclavian
artery. The vertebral artery is divided into four parts;
of this, the third part enters its vertebral course at the
foramen transversarium of six cervical vertebrae to
the posterior aspect of lateral mass of the atlas, the
first cervical vertebrae. The embryogenesis of the
vertebral artery occurs between day 32nd and 40th day
of gestation. They are formed from fusion of the
longitudinal anastomoses which connect the cervical
intersegmental arteries following the course of the
two through eight cervical segmental nerves. The
intersegmental arteries regress during the embryonal
development. Only the 7th intersegmental artery does
not regress and becomes the proximal portion of the
subclavian artery which gives rise to the vertebral
artery.[2] It has been speculated that persistence of
a portion of the primitive dorsal aorta with two
intersegment arteries may give rise to vertebral
artery duplication. Failure on the regression of the
intersegment arteries can result in vertebral artery
fenestration.[3] This fenestration may contribute to the
development of the double foramen transversarium,
but it is not proven yet. The cause of variations on the
size and shape of the foramen transversarium is not
well known. It may be developmental or related to the
variations of the course of vertebral artery.
The vertebral artery enters its course, nearly
always at the foramen transversarium of the sixth
cervical vertebrae. Due to this fact, the foramen
transversarium of the seventh cervical vertebrae
contains only vertebral vein along with nerve
branches. Occasionally, in about 5% of the cases, the
vertebral artery or vein may travel through the foramen
transversarium of the seventh cervical vertebrae.
This is why these seventh foramen transversaria are
usually smaller than the sixth, or even sometimes
absent. The tortuosity of the vertebral artery may
cause bone destruction.[4] Thus, it may be a factor
in the size of the foramina. It also described bony
excavation on the anterior surface of the superior
articular process by pressure of the vertebral artery.
Since the vertebral vessels are a factor in the formation
of the foramen transversarium, it can be assumed
that variations in the presence and course of the
vessels will be manifested in changes of the foramen
transversarium. Conversely, variations of the foramen
transversarium can be useful or estimating changes
or variations of the vessels and accompanying nerve
structures.[5] Similar correlation may be suggested for
double foramen transversarium. One of the foramina
may be occupied by the vertebral artery and the other
by vertebral vein. The left foramen transversarium
is larger than the right foramen transversarium.[6]
It was reported that this vertebral artery enters the
foramen transversarium of vertebral at C6 in 88% of
cases, C7 in only 5%, and C5 in 7% of cases.[7] An
accessory transverse foramen is seen smaller in size
than the primary foramen generally found in the sixth
cervical vertebrae and less frequently in the adjacent
vertebrae.
Anatomy and morphology of foramen transversarium
is useful to the operating spine surgeons and
radiologist in the interpretation of radiographic films
and computed tomogram scans.[8] The presence of
accessory transverse foramen is a rare condition and this
may have variations that affect the course of vertebral
artery. The deformation and variations of the accessory
foramen may affect the anatomical course of vital
vascular and neural structures and consequently cause
pathological conditions are small or even sometimes
absent. Variations in the number and size of the
foramen transversarium of the cervical vertebrae may
result in headache, migraine, and fainting attack due
to compression of the vertebral artery.[9] The vertebral
vessels in such situations may be compressed by head
movements and may give rise to vascular insufficiency.
Clinically, this type of variations is important for the
radiologist while doing computed tomographic and
magnetic resonant imaging scan. These variations of
foramina transversarium are also important for surgeon
during posterior cervical surgery.[10]
MATERIALS AND METHODS
In our research, about 120 cervical vertebrae were
collected from the Department of Anatomy, Saveetha
Medical College, Thandalam, Tamil Nadu. Of which
39 bones were observed with the presence of accessory
foramen transversarium. The details on age, sex, and
race of the individuals from which these vertebrae
were derived were not available. The following
parameters were observed and measured using digital
Vernier caliper.
• Size: Complete, and incomplete.
• Shapes: Round, oval, and irregular.
• Location: Unilateral, bilateral, anterior, posterior,
right, and left.
• Diameter: Anteroposterior and transverse.
• Classication: Brachiomorph, mesomorph, and
dolichomorph.
The shapes, size, and location were concluded based
on the visual observation done in the vertebrae.
Using a digital Vernier caliper, the anteroposterior
and transverse diameters of accessory foramen
transversarium were measured. The transverse
and anteroposterior diameter of each foramen was
calculated to estimate the mean diameter of each
accessory foramen transversarium.

R. Revathy, et al.
439
Drug Invention Today | Vol 11 • Issue 2 • 2019
Statistical evaluations were performed for each
measurement. The mean and standard deviation value
was performed to determine if there was a significant
difference between the right and left side.
OBSERVATION AND RESULTS
In this study, we observed 39 cervical vertebrae with
the presence of accessory transverse foramen of 120
cervical vertebrae. As mentioned in the materials
and methods, we classified the accessory foramen
transversarium based on the following criteria.
Of 39 accessory foramen, 20 are complete (13 on the
right side and 7 on the left side) and 19 are incomplete
(13 on the right side and 9 on the left side). According
to the shape, accessory foramen transversarium is
classified into round, oval, and irregular. Round-
shaped foramen is seen in 11 vertebrae, of which
seven is seen on the right side and five on the left side,
oval-shaped foramen, which is comparatively seen in
more vertebrae, is seen in 18 vertebrae, of which 11 is
seen on the right side and seven on the left side, and
elliptical-shaped one is seen in 10 vertebrae, of which
six right side and four left-sided foramen. Similarly,
the accessory foramen transversarium is divided into
complete and incomplete. In 28 vertebrae, accessory
foramen is observed only on either of one side (17 on
the right side and 11 on the left side) and 11 vertebrae
are observed with bilateral presences of accessory
foramen transversarium [Figure 1].
Anteroposterior diameter is measured and calculated in
39 cervical vertebrae. About 21 foramens are measured
on the right side which is 1.46762 mm ± 0.5235 mm
and on the left side about 18 foramen transversaria
are measured which is 1.51277 mm ± 0.4318 mm.
Likewise, transverse diameter measured in 21
foramina are measured on the right side and its value is
1.8181 mm ± 0.5863 mm and on the left side about 18
foramina are measured and its value is 1.821 ± 0.6363
[Figure 2].
DISCUSSION
The foramen transversarium develops from the
fusion of two components, namely vestigial costal
element and the true transverse process of the
cervical vertebrae. The vertebral vessels and nervous
plexus are caught between these two bony parts. The
foramen transversarium is closed laterally by the
costotransverse bar, a thin plate of bone connecting
the costal element to the original transverse process.
Accessory foramen transversarium might be due to
double costal element on the same side fusing to
the original transverse process resulting in unusual
number of foramen transversarium.[11] The accessory
foramen transversarium may also be due to variations
in the vertebral vessels. The vertebral artery arises
from the subclavian artery and usually traverses
through the foramen transversarium of all cervical
vertebrae except the seventh.[12] The two vertebral
arteries are solely responsible for posterior circulation
of the brain. The tortuous course of vertebral artery
and rarely medial position of transverse foramen in
relation to the joint of Luschka may result in life-
threatening iatrogenic injury following cervical
decompression.[13] The two vertebral arteries are
unequal in size in about 75% of cases. One of them
may be extremely narrow, more so on the right side in
10% of cases. Bow hunter’s stroke is a symptomatic
vertebral-basilar insufficiency caused by stenosis
or occlusion of the vertebral artery with head
rotation.[14] It is a common finding on angiography
that head rotation produces stenosis or occlusion
of a contralateral vertebral artery. The narrowing
of the transverse foramen may predispose patients
to vertebral-basilar insufficiency and thrombus
formation, especially with head rotation. Duplication
of extracranial vertebral artery has been reported in
literature.
Figure 1: (a) Round-shaped foramen, (b) oval-shaped
foramen, (c) elliptical-shaped foramen, (d) complete and
incomplete foramen
a
c
b
d
Figure 2: (a) Unilateral foramen, (b) bilateral foramen,
(c) transverse and anteroposterior diameter, (d) measuring
the diameter using the digital Vernier caliper
a
c
b
d

R. Revathy, et al.
Drug Invention Today | Vol 11 • Issue 2 • 2019
440
Vertebral artery develops from a fusion of longitudinal
anastomoses that link the second to sixth cervical
intersegmental arteries. Most of the intersegmental
arteries regress except the seventh which forms the
origin of vertebral artery. Failure of the occlusion
of intersegmental arteries may be responsible
for duplication fenestrations of vertebral artery.
A duplicate vertebral artery may potentially serve
to protect patients against chemical attacks to the
brain and provide collateral blood flow to the basilar
artery. However, fenestrated vertebral arteries have
been demonstrated histological lyrics to be weak
with irregular elastic fibers in the vessels wall.[15]
Fenestrated/double vertebral arteries may carry more
risk of thrombus formation and embolization, leading
to serve transient ischemic attacks. It is easily
understood that the course of vital vascular and neural
structures, occupying the foramen transversarium,
may be distorted due to variations like the presence
of accessory foramen transversarium. Interestingly,
it has been estimated that up to 10% of malpractice
involving physicians may be due to a lack of knowledge
of the anatomical variations. Thus, detecting and
understanding anatomical variations of the vertebral
artery, accompanying the variations of the foramina
transversaria, are essential while performing the
complex surgical procedures that involve the screw
fixation, to avoid possible complications.
The earliest known study was done by Taitz et al.
(1978) who studied 480 foramina transversaria
and found 34 vertebrae having accessory foramen
transversarium in it. In Sharma et al. observed
accessory foramen transversarium in 16 of 200
cervical vertebrae. Similarly, in 2014, Kattikireddi
et al. studied three accessory foramen transversaria
of 100 cervical vertebrates.[16,17] In our study, we
observed about 39 cervical vertebrae with the
presence of accessory transverse foramen of 120
cervical vertebrae. Out of these 13 complete accessory
foramen transversarium seen in right side and 7 were
on the left side and 13 incomplete accessory foramen
transversarium seen on its right side and 6 were on
the left side of cervical vertebrae Table 1. Laxmi et al.
study observed the double foramen transversarium
in 4.76% of the cases.[18] They studied about 210
cervical vertebrae, in which 10 vertebrae were
found to haveorigin of vertebral artery. Among
10 vertebrae, eight vertebrae were found to have
bilateral and two vertebrae were found to have
unilateral double foramen transversarium. Magi and
Suman study reported 19 (12.6%) vertebrae having
bilateral double transverse foramina of 150 cervical
vertebrae.[19] In our study, we have observed about
11 cervical vertebrae having the bilateral presence of
accessory transverse foramen transversarium. Yadav
et al. observed eight accessory foramen transversaria
which includes three on unilateral and five on bilateral
foramen of 120 cervical vertebrae.[20] In this study, of
120 cervical vertebrae, about 28 cervical vertebrae
have the unilateral presence of accessory foramen
transversarium and 11 having bilateral accessory
foramen transversarium [Table 3]. Sangari et al.
studied the mean diameter of the right transverse
foramen varied from 2.54 mm to 7.79 mm in diameter
(mean=5.55 mm ± 0.87 mm), whereas the mean
diameter of the left transverse foramen varied from
2.65 mm to 7.35 mm (mean=5.48 mm ± 0.77 mm).[21]
In our study, the mean diameter of the right accessory
foramen transversarium varied from 0.5 mm to
2.00 mm, whereas the mean diameter of the left
accessory foramen transversarium varied from
1.5 mm to 2.00 mm Table 4. Apart from transverse
diameter, we also studied about anteroposterior
diameter of accessory foramen transversarium which
is not reported in any literature. The knowledge of
the dimension of both foramen transversarium and
accessory foramen transversarium may contribute
as additional information for the clinical during any
procedure around cervical region.
Taitz et al. and Aziz[22] observed the different shape of
the accessory foramen transversarium such as round,
oval, irregular, and quadrangular. They also reported
that among the shapes, round-shaped foramen were the
most common one (Taitz et al. - 54.8% and Aziz et al.
-54.1%). In this study, we observed only round, oval,
and irregular, we did not observe the quadrangular-
shaped foramen in this study, but in this study, the
common shape of foramen was oval which is 46%.Of
these Oval shape were seen in 18 ,of which 11 were on
the right side and 7 were on the left side.Round shaped
Table 3: Based on location
Classification Right side Left side Total number
Unilateral 17 11 28
Bilateral 11
Table 1: Based on size
Classification Right side Left side Total number
Complete accessory foramen 13 7 20
Incomplete accessory foramen 13 6 19
Table 2: Based on shapes
Classification Right side Left side Total number
Round 7 511
Oval 11 718
Irregular 6410

R. Revathy, et al.
441
Drug Invention Today | Vol 11 • Issue 2 • 2019
foramen were seen in 11 of which, 7 were on the right
side and 5 were on the left side. Irregularly shaped
foramen were seen in 10 of which 6 were on the right
side and 4 were on the left side Table 2. Variations in
the number and size of the foramen transversarium of
the cervical vertebrae are important for the radiologist
and also for neurosurgeon during posterior cervical
surgery.
CONCLUSION
In this study, the presences of accessory foramen
transversarium were found in 39 cervical vertebrae of
120 cervical vertebrae. The reasons for the presences
of accessory foramen transversarium would be
torturous passing of vessels through the cartilaginous
development of cervical vertebrae or improper fusion
of costal element and true transverse process of
cervical vertebrae. The knowledge of the presences
of accessory foramen transversarium is important for
radiologist and clinicians during vascular surgeries
and neurosurgeries.
REFERENCES
1. Collinis P, Wigley C, Gieeson M. Grays Anatomy, the
Anatomical Basis of Clinical Practice. 40th ed. New York:
Churchill Livingston Elseiver; 2008. p. 652-7.
2. Fitzgerald MJ. Human Embryology: A Regional Approach. 1st ed.
New York, USA: HarperCollins College Div.; 1978. p. 38-56.
3. Sim E, Vaccaro AR, Berzlanovich A, Thaler H, Ullrich CG.
Fenestration of the extracranial vertebral artery: Review of the
literature. Spine (Phila Pa 1976) 2001;26:E139-42.
4. Hyyppä SE, Laasonen EM. Erosion of cervical vertebrae caused
by elongated and tortuous vertebral arteries. Neuroradiology
1974;7:49-51.
5. Taitz C, Nathan H, Arensburg B. Anatomical observations of
the foramina transversaria. J Neurol Neurosurg Psychiatry
1978;41:170-6.
6. Epstein NE, Silvergleid R. Magnetic resonance angiographic
diagnosis of ecstatic vertebral artery. J Spinal Disord
1995;8:308-10.
7. Kubikova E, Osvaldova M. A variable origin of vertebral artery.
Bratislaske Lekarske Listy 2008; 109, 28-30.
8. Divya A, Sunita S, Bijaylaxmi P, Kumar HS, Kumar CP.
Variations in foramen transversarium: An osteological in
Eastern India. Int J Curr Res 2012;4:120-2.
9. Caovilla HH, Gananca MM, Silva ML. Sindrome Cervical
Quadros Coto Neurologices Maid Comuns. Vol. 3. Sao Paulo:
Atheneu; 2000. p. 95-100.
10. Kaya S, Yilmaz ND, Pusat S, Kural C, Kirik A, Izci Y, et al.
Double foramen transversarium variation in ancient byzantine
cervical vertebrae: Preliminary report of an anthropological
study. Turk Neurosurg 2011;21:534-8.
11. Veeramani R, Shankar N. An unusual origin of the right
vertebral artery from the thyrocervical trunka case report. Int J
Basic Med Sci 2011;2:2-6.
12. Frazer JE. Cervical vertebrae. In: Anatomy of Human Skeleton.
6th ed. London: J and A Churchill liv td; 1965. p. 21-8.
13. Curylo LJ, Mason HC, Bohlman HH, Yoo JU. Tortuous course
of the vertebral artery and anterior cervical decompression:
A cadaveric and clinical case study. Spine (Phila Pa 1976)
2000;25:2860-4.
14. Seki T, Hida K, Akino M, Iwasaki Y. Anterior decompression
of the atlantoaxial vertebral artery to treat bow hunter’s stroke:
Technical case report. Neurosurgery 2001;49:1474-6.
15. Takasato Y, Hayashi H, Kobayashi T, Hashimoto Y. Duplicated
origin of right vertebral artery with rudimentary and accessory
left vertebral arteries. Neuroradiology 1992;34:287-9.
16. Sharma A, Singh K, Gupta V, Srivastava S. Double foramen
transversarium variation in cervical vertebra an osteological
study. J Anat Soc India 2010;59:229-31.
17. Reddi RS, Setty SN. A study of double foramen transversarium
in dried cervical vertebrae. Int J Health Sci Res 2014;4:59-61.
18. Laxmi C, Shailesh P, Jatin G. Double foramen transversarium
in cervical vertebrae: And clinical importance. Int J Res Med
2013;2:103-5.
19. Magi M, Suman V. A study on variations of foramen
transversarium of cervical vertebrae. Natl J Clin Anat
2014;3:4-7.
20. Yadav Y, Goswami P, Bharihoke V. An osteological study of
foramen transversarium variations and clinical aspects. J Evol
Med Dent Sci 2014;3:14562-6.
21. Sangari SK, Doussous PM, Heineman T. Dimensions and
anatomical variations of the foramen transversarium of typical
cervical vertebrae. Anat Res Int 2015;39:18-23.
22. Aziz JN. Michel Morgan morphological study of the foramen
transversarium of the atlas vertebra among Egyptian population
and its clinical significance. Anat Physiol Biochem Int J
2018;4:1-5.
Source of support: Nil; Conflict of interest: None Declared
Table 4: Based on diameter (mean and standard deviation value)
Classification Right side (total number of bones: 21) Left side (total number of bones: 18)
Anteroposterior diameter 1.4676±0.5235 mm 1.5127±0.4318 mm
Transverse diameter 1.8181±0.5863 mm 1.8210±0.6363 mm